ICES Cooperative Research Report Rapport des Recherches Collectives Cephalopod biology and fisheries in Europe: II. Species Accounts. No. 325 June 2015 ICES COOPERATIVE RESEARCH REPORT RAPPORT DES RECHERCHES COLLECTIVES NO. 325 June 2015 Cephalopod biology and fisheries in Europe: II. Species Accounts Editors Patrizia Jereb • A. Louise Allcock • Evgenia Lefkaditou Uwe Piatkowski • Lee C. Hastie • Graham J. Pierce International Council for the Exploration of the Sea Conseil International pour l’Exploration de la Mer H. C. Andersens Boulevard 44–46 DK-1553 Copenhagen V Denmark Telephone (+45) 33 38 67 00 Telefax (+45) 33 93 42 15 www.ices.dk info@ices.dk Recommended format for purposes of citation: Jereb, P., Allcock, A.L., Lefkaditou, E., Piatkowski, U., Hastie, L.C., and Pierce, G.J. (Eds.) 2015. Cephalopod biology and fisheries in Europe: II. Species Accounts. ICES Cooperative Research Report No. 325. 360 pp. Series Editor: Emory D. Anderson. 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ISBN 978-87-7482-155-7 ISSN 1017-6195 © 2015 International Council for the Exploration of the Sea Contents 1 Executive summary ........................................................................................................ 1 2 General introduction ..................................................................................................... 2 3 2.1 Origins and acknowledgements ........................................................................ 2 2.2 Topics covered by the reviews ........................................................................... 3 Octopus vulgaris Cuvier, 1797 ................................................................................... 14 3.1 Geographic distribution .................................................................................... 14 3.2 Taxonomy ........................................................................................................... 15 3.2.1 Systematics .............................................................................................. 15 3.2.2 Type locality ............................................................................................ 15 3.2.3 Type repository....................................................................................... 15 3.3 Diagnosis ............................................................................................................ 15 3.3.1 Paralarvae ................................................................................................ 15 3.3.2 Juveniles and adults ............................................................................... 16 3.4 Remarks .............................................................................................................. 17 3.5 Life history .......................................................................................................... 18 3.5.1 3.5.2 3.5.3 3.5.4 3.6 Egg and juvenile development ............................................................. 18 Growth and lifespan .............................................................................. 18 Maturation and reproduction ............................................................... 20 Natural mortality.................................................................................... 21 Biological distribution ....................................................................................... 21 3.6.1 Habitat ..................................................................................................... 21 3.6.2 Migrations ............................................................................................... 21 3.7 Trophic ecology.................................................................................................. 21 3.7.1 Prey........................................................................................................... 21 3.7.2 Predators .................................................................................................. 23 3.8 Other ecological aspects .................................................................................... 24 3.8.1 Parasites ................................................................................................... 24 3.8.2 Contaminants .......................................................................................... 25 3.8.3 Environmental effects ............................................................................ 25 4 3.9 Fisheries .............................................................................................................. 26 3.10 Aquaculture ........................................................................................................ 27 3.11 Future research, needs, and outlook ............................................................... 28 Eledone cirrhosa (Lamarck, 1798)............................................................................... 30 4.1 Geographic distribution .................................................................................... 30 4.2 Taxonomy ........................................................................................................... 31 4.2.1 Systematics .............................................................................................. 31 4.2.2 Type locality ............................................................................................ 31 4.2.3 Type repository....................................................................................... 31 4.3 Diagnosis ............................................................................................................ 31 4.3.1 Paralarvae ................................................................................................ 31 4.3.2 Juveniles and adults ............................................................................... 32 4.4 Life history .......................................................................................................... 32 4.4.1 4.4.2 4.4.3 4.4.4 4.5 Egg and juvenile development ............................................................. 33 Growth and lifespan .............................................................................. 33 Maturation and reproduction ............................................................... 35 Natural mortality.................................................................................... 36 Biological distribution ....................................................................................... 36 4.5.1 Habitat ..................................................................................................... 36 4.5.2 Migrations ............................................................................................... 36 4.6 Trophic ecology.................................................................................................. 36 4.6.1 Prey........................................................................................................... 36 4.6.2 Predators .................................................................................................. 37 4.7 Other ecological aspects .................................................................................... 38 4.7.1 4.7.2 4.7.3 4.7.4 5 Parasites ................................................................................................... 38 Contaminants .......................................................................................... 39 Environmental effects ............................................................................ 39 Behaviour ................................................................................................ 39 4.8 Fisheries .............................................................................................................. 39 4.9 Future research, needs, and outlook ............................................................... 41 Eledone moschata (Lamarck, 1798) ............................................................................ 43 5.1 Geographic distribution .................................................................................... 43 5.2 Taxonomy ........................................................................................................... 44 5.2.1 Systematics .............................................................................................. 44 5.2.2 Type locality ............................................................................................ 44 5.2.3 Type repository....................................................................................... 44 5.3 Diagnosis ............................................................................................................ 44 5.3.1 Eggs and hatchlings ............................................................................... 44 5.3.2 Juveniles and adults ............................................................................... 44 5.4 Remarks .............................................................................................................. 45 5.5 Life history .......................................................................................................... 45 5.5.1 Egg and juvenile development ............................................................. 46 5.5.2 Growth and lifespan .............................................................................. 46 5.5.3 Maturation and reproduction ............................................................... 47 5.6 Biological distribution ....................................................................................... 48 5.6.1 Habitat ..................................................................................................... 48 5.6.2 Migrations ............................................................................................... 49 5.7 Trophic ecology.................................................................................................. 49 5.7.1 Prey........................................................................................................... 49 5.7.2 Predators .................................................................................................. 50 5.8 Other ecological aspects .................................................................................... 50 5.8.1 Parasites ................................................................................................... 50 6 5.9 Fisheries .............................................................................................................. 50 5.10 Future research, needs, and outlook ............................................................... 51 Sepia officinalis Linnaeus, 1758 ................................................................................. 53 6.1 Geographic distribution .................................................................................... 53 6.2 Taxonomy ........................................................................................................... 54 6.2.1 Systematics .............................................................................................. 54 6.2.2 Type locality ............................................................................................ 54 6.2.3 Type repository....................................................................................... 54 6.3 Diagnosis ............................................................................................................ 54 6.3.1 Paralarvae and hatchlings ..................................................................... 54 6.3.2 Juveniles and adults ............................................................................... 54 6.4 Remarks .............................................................................................................. 55 6.5 Life history .......................................................................................................... 56 6.5.1 6.5.2 6.5.3 6.5.4 6.6 Egg and juvenile development ............................................................. 56 Growth and lifespan .............................................................................. 57 Maturation and reproduction ............................................................... 59 Natural mortality.................................................................................... 61 Biological distribution ....................................................................................... 61 6.6.1 Habitat ..................................................................................................... 61 6.6.2 Migrations ............................................................................................... 62 6.7 Trophic ecology.................................................................................................. 62 6.7.1 Prey........................................................................................................... 62 6.7.2 Predators .................................................................................................. 65 6.8 Other ecological aspects .................................................................................... 67 6.8.1 Parasites ................................................................................................... 67 6.8.2 Contaminants .......................................................................................... 68 6.8.3 Behaviour ................................................................................................ 68 7 6.9 Fisheries .............................................................................................................. 68 6.10 Aquaculture ........................................................................................................ 71 6.11 Future research, needs, and outlook ............................................................... 72 Sepia elegans Blainville, 1827 ..................................................................................... 74 7.1 Geographic distribution .................................................................................... 74 7.2 Taxonomy ........................................................................................................... 75 7.2.1 Systematics .............................................................................................. 75 7.2.2 Type locality ............................................................................................ 75 7.2.3 Type repository....................................................................................... 75 7.3 Diagnosis ............................................................................................................ 75 7.3.1 Paralarvae ................................................................................................ 75 7.3.2 Juveniles and adults ............................................................................... 75 7.4 Remarks .............................................................................................................. 77 7.5 Life history .......................................................................................................... 77 7.5.1 Egg and juvenile development ............................................................. 77 7.5.2 Growth and lifespan .............................................................................. 77 7.5.3 Maturation and reproduction ............................................................... 78 7.6 Biological distribution ....................................................................................... 79 7.6.1 Habitat ..................................................................................................... 79 7.6.2 Migrations ............................................................................................... 79 7.7 Trophic ecology.................................................................................................. 80 7.7.1 Prey........................................................................................................... 80 7.7.2 Predators .................................................................................................. 80 7.8 Other ecological aspects .................................................................................... 81 7.8.1 Parasites ................................................................................................... 81 7.8.2 Contaminants .......................................................................................... 81 8 7.9 Fisheries .............................................................................................................. 81 7.10 Future research, needs, and outlook ............................................................... 82 Sepia orbignyana Férussac in d’Orbigny, 1826 ....................................................... 84 8.1 Geographic distribution .................................................................................... 84 8.2 Taxonomy ........................................................................................................... 85 8.2.1 Systematics .............................................................................................. 85 8.2.2 Type locality ............................................................................................ 85 8.2.3 Type repository....................................................................................... 85 8.3 Diagnosis ............................................................................................................ 85 8.3.1 Paralarvae ................................................................................................ 85 8.3.2 Juveniles and adults ............................................................................... 85 8.4 Remarks .............................................................................................................. 86 8.5 Life history .......................................................................................................... 86 8.5.1 Egg and juvenile development ............................................................. 87 8.5.2 Growth and lifespan .............................................................................. 87 8.5.3 Maturation and reproduction ............................................................... 88 8.6 Biological distribution ....................................................................................... 88 8.6.1 Habitat ..................................................................................................... 88 8.6.2 Migrations ............................................................................................... 89 8.7 Trophic ecology.................................................................................................. 89 8.7.1 Prey........................................................................................................... 89 8.7.2 Predators .................................................................................................. 90 8.8 Other ecological aspects .................................................................................... 90 8.8.1 Contaminants .......................................................................................... 90 8.8.2 Biochemistry ........................................................................................... 90 9 8.9 Fisheries .............................................................................................................. 90 8.10 Future research, needs, and outlook ............................................................... 91 Sepietta oweniana (d’Orbigny, 1841) ........................................................................ 93 9.1 Geographic distribution .................................................................................... 93 9.2 Taxonomy ........................................................................................................... 94 9.2.1 Systematics .............................................................................................. 94 9.2.2 Type locality ............................................................................................ 94 9.2.3 Type repository....................................................................................... 94 9.3 Diagnosis ............................................................................................................ 94 9.3.1 Paralarvae ................................................................................................ 94 9.3.2 Juveniles and adults: .............................................................................. 95 9.4 Remarks .............................................................................................................. 96 9.5 Life history .......................................................................................................... 97 9.5.1 Egg and juvenile development ............................................................. 97 9.5.2 Growth and lifespan .............................................................................. 98 9.5.3 Maturation and reproduction ............................................................... 99 9.6 Biological distribution ..................................................................................... 101 9.6.1 Habitat ................................................................................................... 101 9.6.2 Migrations ............................................................................................. 102 9.7 Trophic ecology................................................................................................ 102 9.7.1 Prey......................................................................................................... 102 9.7.2 Predators ................................................................................................ 103 10 9.8 Other ecological aspects .................................................................................. 104 9.9 Fisheries ............................................................................................................ 104 9.10 Future research, needs, and outlook ............................................................. 104 Sepiola atlantica d’Orbigny, 1842 ........................................................................... 106 10.1 Geographic distribution .................................................................................. 106 10.2 Taxonomy ......................................................................................................... 107 10.2.1 Systematic .............................................................................................. 107 10.2.2 Type locality .......................................................................................... 107 10.2.3 Type repository..................................................................................... 107 10.3 Diagnosis .......................................................................................................... 107 10.3.1 Paralarvae .............................................................................................. 107 10.3.2 Juveniles and adults ............................................................................. 107 10.4 Remarks ............................................................................................................ 108 10.5 Life history ........................................................................................................ 109 10.5.1 Egg and juvenile development ........................................................... 109 10.5.2 Growth and lifespan ............................................................................ 109 10.5.3 Maturation and reproduction ............................................................. 110 10.6 Biological distribution ..................................................................................... 111 10.6.1 Habitat ................................................................................................... 111 10.6.2 Migrations ............................................................................................. 111 10.7 Trophic Ecology ............................................................................................... 112 10.7.1 Prey......................................................................................................... 112 10.7.2 Predators ................................................................................................ 112 10.8 Other ecological aspects .................................................................................. 112 10.8.1 Behaviour .............................................................................................. 112 10.9 Fisheries ............................................................................................................ 113 10.10 Aquaculture ...................................................................................................... 113 10.11 Future research, needs, and outlook ............................................................. 113 11 Loligo vulgaris Lamarck, 1798.................................................................................. 115 11.1 Geographic distribution .................................................................................. 115 11.2 Taxonomy ......................................................................................................... 116 11.2.1 Systematics ............................................................................................ 116 11.2.2 Type locality .......................................................................................... 116 11.2.3 Type repository..................................................................................... 116 11.3 Diagnosis .......................................................................................................... 117 11.3.1 Paralarvae .............................................................................................. 117 11.3.2 Juveniles and adults ............................................................................. 117 11.4 Remarks ............................................................................................................ 117 11.5 Life history ........................................................................................................ 118 11.5.1 Egg and juvenile development ........................................................... 118 11.5.2 Growth and lifespan ............................................................................ 120 11.5.3 Maturation and reproduction ............................................................. 123 11.6 Biological distribution ..................................................................................... 126 11.6.1 Habitat ................................................................................................... 126 11.6.2 Migrations ............................................................................................. 127 11.7 Trophic ecology................................................................................................ 128 11.7.1 Prey......................................................................................................... 128 11.7.2 Predators ................................................................................................ 130 11.8 Other ecological aspects .................................................................................. 132 11.8.1 Parasites ................................................................................................. 132 11.8.2 Contaminants ........................................................................................ 132 11.9 Fisheries ............................................................................................................ 132 11.10 Future research, needs, and outlook ............................................................. 134 12 Loligo forbesii Steenstrup, 1856 ............................................................................... 137 12.1 Geographic distribution .................................................................................. 137 12.2 Taxonomy ......................................................................................................... 138 12.2.1 Systematics ............................................................................................ 138 12.2.2 Type locality .......................................................................................... 138 12.2.3 Type repository..................................................................................... 138 12.3 Diagnosis .......................................................................................................... 138 12.3.1 Paralarvae .............................................................................................. 138 12.3.2 Juveniles and adults ............................................................................. 139 12.4 Life history ........................................................................................................ 139 12.4.1 Egg and juvenile development ........................................................... 139 12.4.2 Growth and lifespan ............................................................................ 141 12.4.3 Maturation and reproduction ............................................................. 144 12.5 Biological distribution ..................................................................................... 146 12.5.1 Habitat ................................................................................................... 146 12.5.2 Migrations ............................................................................................. 147 12.6 Trophic ecology................................................................................................ 148 12.6.1 Prey......................................................................................................... 148 12.6.2 Predators ................................................................................................ 151 13 12.7 Fisheries ............................................................................................................ 152 12.8 Future research, needs, and outlook ............................................................. 153 Alloteuthis subulata (Lamarck, 1798) ..................................................................... 156 13.1 Geographic distribution .................................................................................. 156 13.2 Taxonomy ......................................................................................................... 157 13.2.1 Systematics ............................................................................................ 157 13.2.2 Type locality .......................................................................................... 157 13.2.3 Type repository..................................................................................... 157 13.3 Diagnosis .......................................................................................................... 158 13.3.1 Paralarvae .............................................................................................. 158 13.3.2 Juveniles and adults ............................................................................. 158 13.4 Remarks ............................................................................................................ 159 13.5 Life history ........................................................................................................ 160 13.5.1 Egg and juvenile development ........................................................... 160 13.5.2 Growth and lifespan ............................................................................ 160 13.5.3 Maturation and reproduction ............................................................. 161 13.6 Biological distribution ..................................................................................... 162 13.6.1 Habitat ................................................................................................... 162 13.6.2 Migrations ............................................................................................. 162 13.7 Trophic ecology................................................................................................ 163 13.7.1 Prey......................................................................................................... 163 13.7.2 Predators ................................................................................................ 163 13.8 Other aspects of biology and ecology ........................................................... 164 13.8.1 Parasites ................................................................................................. 164 13.8.2 Behaviour .............................................................................................. 165 13.9 Fisheries ............................................................................................................ 165 13.10 Future research, needs, and outlook ............................................................. 165 14 Alloteuthis media (Linnaeus, 1758) ......................................................................... 168 14.1 Geographic distribution .................................................................................. 168 14.2 Taxonomy ......................................................................................................... 169 14.2.1 Systematics ............................................................................................ 169 14.2.2 Type locality .......................................................................................... 169 14.2.3 Type repository..................................................................................... 169 14.3 Diagnosis .......................................................................................................... 170 14.3.1 Paralarvae .............................................................................................. 170 14.3.2 Juveniles and adults ............................................................................. 170 14.4 Remarks ............................................................................................................ 170 14.5 Life history ........................................................................................................ 171 14.5.1 Egg and juvenile development ........................................................... 171 14.5.2 Growth and lifespan ............................................................................ 172 14.5.3 Maturation and reproduction ............................................................. 173 14.6 Biological distribution ..................................................................................... 174 14.6.1 Habitat ................................................................................................... 174 14.6.2 Migrations ............................................................................................. 174 14.7 Trophic ecology................................................................................................ 174 14.7.1 Prey......................................................................................................... 174 14.7.2 Predators ................................................................................................ 174 14.8 Other ecological aspects .................................................................................. 175 14.8.1 Parasites ................................................................................................. 175 14.9 Fisheries ............................................................................................................ 175 14.10 Future research, needs, and outlook ............................................................. 176 15 Illex coindetii (Vérany, 1839) .................................................................................... 178 15.1 Geographic distribution .................................................................................. 178 15.2 Taxonomy ......................................................................................................... 179 15.2.1 Systematics ............................................................................................ 179 15.2.2 Type locality .......................................................................................... 179 15.2.3 Type repository..................................................................................... 179 15.3 Diagnosis .......................................................................................................... 179 15.3.1 Paralarvae .............................................................................................. 179 15.3.2 Juveniles and adults ............................................................................. 180 15.4 Remarks ............................................................................................................ 180 15.5 Life history ........................................................................................................ 181 15.5.1 Egg and juvenile development ........................................................... 181 15.5.2 Growth and lifespan ............................................................................ 182 15.5.3 Maturation and reproduction ............................................................. 184 15.6 Biological distribution ..................................................................................... 185 15.6.1 Habitat ................................................................................................... 185 15.6.2 Migrations ............................................................................................. 186 15.7 Trophic ecology................................................................................................ 186 15.7.1 Prey......................................................................................................... 186 15.7.2 Predators ................................................................................................ 188 15.8 Other ecological aspects .................................................................................. 190 15.8.1 Parasites ................................................................................................. 190 15.8.2 Environmental effects .......................................................................... 190 15.9 Fisheries ............................................................................................................ 191 15.10 Future research, needs, and outlook ............................................................. 192 16 Todarodes sagittatus (Lamarck, 1798) .................................................................... 194 16.1 Geographic distribution .................................................................................. 194 16.2 Taxonomy ......................................................................................................... 195 16.2.1 Systematics ............................................................................................ 195 16.2.2 Type locality .......................................................................................... 195 16.2.3 Type repository..................................................................................... 195 16.3 Diagnosis .......................................................................................................... 196 16.3.1 Paralarvae .............................................................................................. 196 16.3.2 Juveniles and adults ............................................................................. 196 16.4 Life history ........................................................................................................ 197 16.4.1 Egg and juvenile development ........................................................... 197 16.4.2 Growth and lifespan ............................................................................ 197 16.4.3 Maturation and reproduction ............................................................. 198 16.5 Biological distribution ..................................................................................... 199 16.5.1 Habitat ................................................................................................... 199 16.5.2 Migrations ............................................................................................. 199 16.6 Trophic ecology................................................................................................ 199 16.6.1 Prey......................................................................................................... 199 16.6.2 Predators ................................................................................................ 202 16.7 Other ecological aspects .................................................................................. 203 16.7.1 Parasites ................................................................................................. 203 16.7.2 Environmental effects .......................................................................... 203 17 16.8 Fisheries ............................................................................................................ 204 16.9 Future research, needs, and outlook ............................................................. 205 Todaropsis eblanae (Ball, 1841) ................................................................................ 207 17.1 Geographic distribution .................................................................................. 207 17.2 Taxonomy ......................................................................................................... 208 17.2.1 Systematics ............................................................................................ 208 17.2.2 Type locality .......................................................................................... 208 17.2.3 Type repository..................................................................................... 208 17.3 Diagnosis .......................................................................................................... 208 17.3.1 Paralarvae .............................................................................................. 208 17.3.2 Juveniles and adults ............................................................................. 209 17.4 Life history ........................................................................................................ 210 17.4.1 Egg and juvenile development ........................................................... 210 17.4.2 Growth and lifespan ............................................................................ 210 17.4.3 Maturation and reproduction ............................................................. 212 17.5 Biological distribution ..................................................................................... 213 17.5.1 Habitat ................................................................................................... 213 17.5.2 Migrations ............................................................................................. 214 17.6 Trophic ecology................................................................................................ 214 17.6.1 Prey......................................................................................................... 214 17.6.2 Predators ................................................................................................ 215 17.7 Other ecological aspects .................................................................................. 216 17.7.1 Parasites ................................................................................................. 216 17.7.2 Environmental effects .......................................................................... 216 17.8 Fisheries ............................................................................................................ 217 17.9 Stock identity .................................................................................................... 217 17.10 Future research, needs, and outlook ............................................................. 218 18 Ommastrephes bartramii (Lesueur, 1821) .............................................................. 220 18.1 Geographic distribution .................................................................................. 220 18.2 Taxonomy ......................................................................................................... 221 18.2.1 Systematics ............................................................................................ 221 18.2.2 Type locality .......................................................................................... 221 18.2.3 Type repository..................................................................................... 221 18.3 Diagnosis .......................................................................................................... 221 18.3.1 Paralarvae .............................................................................................. 221 18.3.2 Juveniles and adults ............................................................................. 222 18.4 Remarks ............................................................................................................ 223 18.5 Life history ........................................................................................................ 224 18.5.1 Egg and juvenile development ........................................................... 224 18.5.2 Growth and lifespan ............................................................................ 224 18.5.3 Maturation and reproduction ............................................................. 225 18.6 Biological distribution ..................................................................................... 226 18.6.1 Habitat ................................................................................................... 226 18.6.2 Migrations ............................................................................................. 226 18.7 Trophic ecology................................................................................................ 226 18.7.1 Prey......................................................................................................... 226 18.7.2 Predators ................................................................................................ 227 18.8 Other ecological aspects .................................................................................. 227 18.8.1 Parasites ................................................................................................. 227 18.8.2 Environmental effects .......................................................................... 228 18.9 Fisheries ............................................................................................................ 228 18.10 Stock identity .................................................................................................... 228 18.11 Future research, needs, and outlook ............................................................. 228 19 Gonatus fabricii (Lichtenstein, 1818) ...................................................................... 230 19.1 Geographic distribution .................................................................................. 230 19.2 Taxonomy ......................................................................................................... 231 19.2.1 Systematics ............................................................................................ 231 19.2.2 Type locality .......................................................................................... 231 19.2.3 Type repository..................................................................................... 231 19.3 Diagnosis .......................................................................................................... 231 19.3.1 Paralarvae .............................................................................................. 231 19.3.2 Juveniles and adults ............................................................................. 232 19.4 Remarks ............................................................................................................ 232 19.5 Life history ........................................................................................................ 233 19.5.1 Egg and juvenile development ........................................................... 233 19.5.2 Growth and lifespan ............................................................................ 233 19.5.3 Maturation and reproduction ............................................................. 234 19.6 Biological distribution ..................................................................................... 235 19.6.1 Habitat ................................................................................................... 235 19.6.2 Migrations ............................................................................................. 235 19.7 Trophic ecology................................................................................................ 235 19.7.1 Prey......................................................................................................... 235 19.7.2 Predators ................................................................................................ 236 19.8 Fisheries ............................................................................................................ 237 19.9 Stock identity .................................................................................................... 237 19.10 Future research, needs, and outlook ............................................................. 238 20 References ................................................................................................................... 239 20.1 Cited references................................................................................................ 239 20.2 Additional references ...................................................................................... 313 20.2.1 Generic references ................................................................................ 313 20.2.2 Octopus vulgaris ..................................................................................... 317 20.2.3 Eledone cirrhosa ...................................................................................... 323 20.2.4 Eledone moschata .................................................................................... 323 20.2.5 Sepia officinalis........................................................................................ 324 20.2.6 Sepia elegans ........................................................................................... 326 20.2.7 Sepia orbignyana ..................................................................................... 327 20.2.8 Sepietta oweniana .................................................................................... 328 20.2.9 Sepiola atlantica ...................................................................................... 328 20.2.10 Loligo vulgaris ................................................................................... 328 20.2.11 Loligo forbesii ..................................................................................... 329 20.2.12 Alloteuthis subulata ........................................................................... 330 20.2.13 Alloteuthis media ............................................................................... 331 20.2.14 Illex coindetii ...................................................................................... 331 20.2.15 Todarodes sagittatus .......................................................................... 332 20.2.16 Todaropsis eblanae ............................................................................. 334 20.2.17 Ommastrephes bartrami ..................................................................... 336 20.2.18 Gonatus fabricii .................................................................................. 337 Annex 1: European and Mediterranean common names for cephalopods .............. 340 Annex 2: Regression equations used to estimate cephalopod sizes based on measurements of beaks............................................................................................. 354 Author and editor contact information .......................................................................... 357 Cephalopod biology and fisheries in Europe: II. Species Accounts 1 | 1 Executive summary This report summarizes current knowledge on the identification, geographical distribution, nomenclature, taxonomy, life history, ecology, and exploitation of cephalopod species of interest to fisheries in European waters. The 17 species range from those currently of significant fishery importance and targeted in at least part of their range (Octopus vulgaris, Sepia officinalis, Loligo vulgaris, Loligo forbesii), through those regularly landed as bycatch (Todaropsis eblanae, Illex coindetii, Eledone cirrhosa, Eledone moschata, Todarodes sagittatus), to those of minor and/or local importance (Alloteuthis subulata, Alloteuthis media, Sepia orbignyana, Sepia elegans, Sepietta oweniana, Sepiola atlantica, Ommastrephes bartramii, Gonatus fabricii). The species reviews aim to provide a concise yet comprehensive account of each, while remaining distinctive from previous and recent accounts. For most of these species, taxonomic status is well resolved, exceptions being the Alloteuthis species. There is less clarity about the existence of discrete stocks, although unsurprisingly this relates to the extent of mobility seen in each species. In addition, the superficial morphological similarities of several species make it difficult for a lay person to distinguish them, and indeed create presently unresolved issues for fishery sampling. The species include benthic, demersal, and pelagic forms, although the existence of horizontal and vertical migrations sometimes tests the limits of such terminology. Most species have a planktonic paralarval phase, although some have hatchlings that immediately adopt a benthic lifestyle. Almost all have annual life cycles, although with a seasonality that varies between both species and regions, and show rapid growth. Most have significant ecological roles as prey and predator, and the high production-to-biomass ratio likely means that their importance is greater than might be indicated from standing stock sizes. However, difficulties with identifying cephalopod remains (identification of their chitnous mandibles is a specialized skill) limit the quality of data on predation. Some information is available on habitat requirements, contaminant burdens, and parasites of these species. Despite the importance of several species for European fisheries, there is limited management of the fisheries and no routine assessment; data collection is often either not part of routine fishery data collection or the data are inadequate for assessment. Increasingly, however, cephalopods are seen as alternative target species to replace overexploited finfish stocks, and the growing fishing effort means that management will almost certainly be needed within the next few years. Also on the horizon is the development of commercial aquaculture, especially for Octopus vulgaris. 2 | 2 ICES Cooperative Research Report No. 325 General introduction Graham J. Pierce, A. Louise Allcock, and Patrizia Jereb 2.1 Origins and acknowledgements This is the second ICES Cooperative Research Report on cephalopods, the first having been published in 2010 (Pierce et al., 2010). Like the first report, it is based on material originally assembled during the CEPHSTOCK project (Cephalopod Stocks in European Waters: Review, Analysis, Assessment and Sustainable Management, Q5CA2002 - 00962, 2002 – 2005). That, in turn, arose from a series of European collaborative research and fishery-data-collection projects over the preceding decade, notably three large-scale projects coordinated by the late Peter Boyle. For the present report, we started with a set of species reviews originally prepared for Workpackage 5 of the CEPHSTOCK project on the life cycle, ecology, and migrations of the main cephalopod species of commercial importance in European waters. These have been expanded, updated, and extensively reworked. Both the original and the revised species accounts are multi-authored works and represent the combined input of many colleagues. Editorial work on the 2005 accounts was coordinated by Uwe Piatkowski and Karsten Zumholz, with contributions from many members of the project team. It was always the intent to publish the reviews, but since CEPHSTOCK ended, such work has been unfunded and their completion has been a protracted process. Responsibility for updating and publishing the reviews passed to the ICES Working Group on Cephalopod Fisheries and Life History, being formally incorporated into its terms of reference in 2008 and leading to a Council Resolution to deliver the work as an ICES Cooperative Research Report. A plan for completion was drawn up, new lead authors were assigned to each chapter, and significant revisions were undertaken. However, by 2010, it was evident that the accounts were already somewhat out of date and work was needed to harmonize chapter format, so a new round of revisions was instigated. The then core editorial team (Patrizia Jereb, Graham Pierce, Louise Allcock, and Evgenia Lefkaditou) met at the Institute for Environmental Protection and Research in Rome in August 2012 to finish drafting the chapters. This was followed by further exchanges with authors, refereeing, and subsequent revisions. A final editorial meeting (with Patrizia Jereb, Louise Allcock, and Graham Pierce) was held at the National University of Ireland, Galway, in December 2013. The final list of authors for the report is as follows: Cleopatra Alidromiti, A. Louise Allcock, Eduardo Balguerias, Paola Belcari, Teresa Borges, Manuel Garcia Tasende, Angel F. González, Angel Guerra, Lee C. Hastie, José Iglesias, Patrizia Jereb, Oleg Katugin, Noussithé Koueta, Drosos Koutsoubas, Evgenia Lefkaditou, Ana Moreno, Daniel Oesterwind, João Pereira, Uwe Piatkowski, Graham J. Pierce, Jean-Paul Robin, Pilar Sánchez, M. Begoña Santos, Paolo Sartor, Sonia Seixas, Jennifer M. Smith, Ignacio Sobrino, Antonio Sykes, Tooraj Valinassab, Roger Villanueva, Sansanee Wangvoralak, and Karsten Zumholz. This report covers not only the main cephalopod species of commercial interest in European waters (Sepia officinalis, Octopus vulgaris, Loligo vulgaris, and Loligo forbesii), but also those species of lesser value that are landed routinely, at least in some parts of Europe (Todaropsis eblanae, Illex coindetii, Eledone cirrhosa, and Eledone moschata), species of previous fishery importance and present local interest (Todarodes sagittatus), and those that are sometimes landed with other species and may occasionally or in specific areas be marketed separately (Alloteuthis subulata, Alloteuthis media, Ommastrephes bar- Cephalopod biology and fisheries in Europe: II. Species Accounts | 3 trami, Sepia elegans, Sepia orbignyana, Sepietta oweniana, Sepiola atlantica). Finally, we include Gonatus fabricii, a species exploited locally for bait, but also identified as having potential commercial fishery value and of high ecological importance as prey of many top predators in the Northeast Atlantic. The biology and ecology of several of the species covered here were previously reviewed in Boyle (1983a). Updated, but brief, descriptions of these and several other European cephalopod species were included in a review paper by Hastie et al. (2009a), and short accounts also appeared within the previous CRR (Pierce et al., 2010). In addition, the FAO has published the first thee volumes of the updated version of “Cephalopods of the World” (see Roper et al., 1984; Jereb and Roper, 2005, 2010; Jereb et al., 2014), reviewing the biology, ecology, and fisheries information on living cephalopod species. Finally, two new volumes of species reviews for important squid species around the world (Rosa et al., 2013a, b) were proposed and completed during the process of compiling the present work. Some squid species accounts from the original CEPHSTOCK report and earlier drafts of the present report chapters were used as source material for the more discursive accounts that appeared in Rosa et al. (2013a, b), and as far as possible, this shared provenance has been made explicit (see e.g. Pierce et al., 2013); however, we wish to state that any unacknowledged overlap arises from the use of material from earlier versions of the present work as source material. We acknowledge the valuable input of our team of referees (Alexander Arkhipkin, Sigurd von Boletzky, Luca Ceriola, Earl Dawe, Elaina Jorgensen, Oleg Katugin, Svjetlana Krstulović Šifner, Vladimir Laptikhovsky, Marek Lipiński, Chingis M. Nigmatullin, and Marion Nixon) as well as the advice from other colleagues, notably Eric Hochberg. We also thank the colleagues who supported us with literature supply and searching, notably Danila Cuccu, Paula Rothman, and Henrik Larsen. For their valuable input to Annex 1, we thank Rita Cannas, Charis Charilaou, Dor Edelist, Jorge Fernandez, Eilif Gaard, Angélique Jadaud, Georgs Kornilovs, Svjetlana Krstulović Šifner, Hatem Hanafy Mahmoud, Jan Mees, Constantine Mifsud, Chingis Nigmatullin, Wahid Refes, Alp Salman, Petri Suuronen, Terje van der Meeren, and Francesca Vitale. All factual errors, however, are the responsibility of the editors and authors. Sources for photographs have been acknowledged in the figure legends, except for the front cover photos for each species, which were provided by E. Beccornia, Manuel E. Garci, Evgenia Lefkaditou, Takashi Okutani, Uwe Piatkowski and Karsten Zumholz. Armin Form designed the artwork with the seven cephalopod images used on the first page of each review as well as the template for the distribution maps. Finally, we acknowledge the great patience shown by ICES staff during the long gestation of this work and, in particular, the editorial input from Emory Anderson, Andrew Payne and Katie Rice Eriksen. 2.2 Topics covered by the reviews The accounts included in the present volume follow a series of standard headings, as described below, illustrated with relevant drawings and photographs, and are designed to be easy to follow. They provide more detail than was possible in the FAO volumes, with specific focus on European species of interest to fisheries. As noted above, detailed information on distribution has been assembled. In addition, although not representing exhaustive literature reviews, the content aims to provide a concise, structured, and reasonably comprehensive summary of our current understanding of the biology and ecology of these species. These new reviews also specifically address the status of exploitation of these cephalopod species by capture fisheries and, in some cases, aquaculture. 4 | ICES Cooperative Research Report No. 325 We adopted a common format for the reviews, but allowing flexibility in relation to additional subheadings within the longer species accounts. The topics covered are summarized below. Common names and synonyms In the main text, we give common names (if any) in use in those European countries with the most important cephalopod fisheries (France, Greece, Italy, Portugal, Spain, and the UK). Where the name given by the FAO differs from the generally accepted common name, we usually provide both. Common names used in other European countries, including names in national and important regional languages, are listed in Annex 1. Generally speaking, the various junior synonyms have fallen out of regular use; the exception is Loligo forbesi for Loligo forbesii. Most authors for this species, from Joubin (1895) to the present day, have used “forbesi”. However, Steenstrup (1856) clearly states that he named the species after Professor Edward Forbes and consistently used “forbesii” in his manuscript. Here, we follow a recent review by Allcock (2010) and also the FAO catalogue (Jereb and Roper, 2010) in accepting Steenstrup’s original name. Geographic distribution The original starting point for these descriptions of the species’ ranges was the relevant entry in the FAO “Cephalopods of the World”, augmented with additional relevant information for European waters. However, information on the geographical distribution of these species was re-evaluated for the recently published FAO guides (Jereb and Roper, 2005, 2010), and has been further reviewed and updated for inclusion in the present volume, providing the most comprehensive summaries of distribution available to date. New maps are provided. As some of the detailed information available is ambiguous or contradictory in relation to species range, however, the maps should be treated as a general guide, with details being provided in the text. It became evident during the review process that many past accounts of distribution are contradictory, sometimes reflecting errors in published sources or in citations thereof, and on other occasions indicating temporary or permanent shifts in species distribution. In addition, there is clearly an issue of what constitutes the “usual” range and which records, therefore, represent occasional excursions beyond the normal range. Our approach here has been to present maps representing the usual distribution, but providing clarification and detailing issues and exceptions within the report text. Within the text, we generally use local spellings, including accented characters, because knowing the correct local spelling makes it easier to search digital resources for additional information for that area. Mediterranean Sea The present report concerns cephalopod species of both the Northeast Atlantic and the Mediterranean Sea. We have assumed that readers are familiar with the geography of the Northeast Atlantic. However, because the Mediterranean lies outside the ICES Area, we provide a description here. The Mediterranean Sea is a body of water almost completely enclosed by land, a characteristic from which its name derives (from the Latin mediterraneus, meaning "in the middle of the land"). It extends from the Strait of Gibraltar in the west to the Dardanelli entrance and the Suez Canal in the north and southeast, respectively, covering an area of ca. 2.5 million km2. It connects to the Atlantic Ocean in the west through the Strait Cephalopod biology and fisheries in Europe: II. Species Accounts | 5 of Gibraltar, a threshold only 14 km wide, to the Sea of Marmara in the northeast, and through this to the Black Sea by means of the Strait of Bosphorus. The Suez Canal now connects the Mediterranean to the Indian Ocean. Following the International Hydrographic Organization (IHO, 1953), it is divided into two deep basins, western and eastern, separated by an ideal line connecting Cape Lilibeo (western Sicily) to Cape Bon (Tunisia), and subdivided into a number of smaller waterbodies, each with its own designation. Accordingly, from west to east, the following areas are recognized: the Strait of Gibraltar, the Alboran Sea (between Spain and Morocco), the Balearic Sea (between mainland Spain and its Balearic islands), the Ligurian Sea (between Corsica and Liguria, northern Italy), the Tyrrhenian Sea (enclosed by Sardinia, the Italian peninsula, and Sicily), the Ionian Sea (between Italy, Albania, and Greece), the Adriatic Sea (between Italy, Slovenia, Croatia, Bosnia and Herzegovina, Montenegro, and Albania), and the Aegean Sea (between Greece and Turkey). In addition, there are some other areas of the Mediterranean whose names have been in common use since ancient times and that remain in use today. Among these, the following are worth mentioning, given their association with fisheries-related issues: the Sea of Sardinia, as a part of the Balearic Sea (between Sardinia and the Balearic Islands); the Sea of Sicily (between Sicily and Tunisia), also known as the Strait of Sicily (Cleveland, 1989); the Libyan Sea (between Libya and Crete); the Thracian Sea and the Sea of Crete in the Aegean Sea; and the Levantine Sea, the easternmost area of the Mediterranean. A further subdivision has been considered in recent years as a practical working approach (GFCM, 2007): western Mediterranean (Algeria, France, Morocco, and Spain); central Mediterranean (Albania, Croatia, Italy, Libya, Malta, Montenegro – reported as Serbia and Montenegro before 2008, and Tunisia); and eastern Mediterranean [Cyprus, Egypt, Gaza Strip, and West Bank (Palestine), Greece, Israel, Lebanon, and Syria]. This working subdivision has been taken into account in reporting FAO fisheries statistics. Taxonomy The taxonomy of some groups of Cephalopoda (e.g. Loliginidae) has undergone extensive revision in recent years, whereas that of other groups has remained reasonably stable. We have attempted to use correct nomenclature throughout, based on the most recent taxonomic revisions. Detailed information on taxonomy and nomenclature was given for some of the species included herein in Allcock (2010). For those species, we continue to use the same nomenclature, which is still considered correct, although we have omitted subgeneric classifications for the sepiids. The species are as follows: 1. Octopus vulgaris Cuvier, 1797 2. Eledone cirrhosa (Lamarck, 1798) 3. Eledone moschata (Lamarck, 1798) 4. Sepia officinalis Linnaeus, 1758 5. Sepia elegans Blainville, 1827 6. Sepia orbignyana Férussac in d’Orbigny, 1826 7. Loligo vulgaris Lamarck, 1798 8. Loligo forbesii Steenstrup, 1856 9. Alloteuthis subulata (Lamarck, 1798) 10. Alloteuthis media (Linnaeus, 1758) 11. Illex coindetii (Verany, 1839) 6 | ICES Cooperative Research Report No. 325 12. Todarodes sagittatus (Lamarck, 1798) 13. Todaropsis eblanae (Ball, 1841) With the exception of the species of Alloteuthis, these taxa are well defined and relatively easy to identify. Alloteuthis is problematic, although the validity of the genus has recently been confirmed (Vecchione et al., 2005). However, molecular data from three loci (two mitochondrial and one nuclear) sequenced in samples sourced from across the geographic range of Alloteuthis show that relative tail length, which is commonly used to identify European species, does not separate the species (Anderson et al., 2008). The sequence data confirm the presence of two distinct European species nonetheless. However, the type specimens of A. subulata and A. media cannot be found by the institutes thought to house them, which makes progress difficult in delimiting the species. Redescriptions and neotype designations (if the original types cannot be located) are essential. More recently, morphological characters have been described that appear to effectively delimit the species. The arm length as a fraction of anterior mantle length (measured from the fin’s upper edge to the mantle opening) ranges between 81 and 167% in one species (purportedly A. media) and between 25 and 52% in the other (purportedly A. subulata) (Lefkaditou et al., 2012). Further detailed morphological work coupled with molecular genetics is required to confirm the extent of both species. Although we treat the species separately herein, it is very difficult to know which species (A. media, A. subulata, or a mixture of the two) was actually being studied in older papers, and much basic work will need to be repeated in future studies to understand how the biology of the two species differs. Further details of the taxonomic issues are considered in each of the species accounts. In addition to those listed above, the other four species included are: 14. Sepietta oweniana (d'Orbigny, 1841) 15. Sepiola atlantica d’Orbigny, 1842 16. Ommastrephes bartramii (Lesueur, 1821) 17. Gonatus fabricii (Lichtenstein, 1818) The oegopsids O. bartramii and G. fabricii are well defined. Most nomenclatural issues revolve around the use of a single –i or double –ii at the end of the specific epithets. This depends on how the original authority constructed the name, and in both cases here, -ii is the correct ending, as used by Lesueur (1821) and Lichtenstein (1818) in their original descriptions. Sepietta oweniana (d'Orbigny, 1841) is also well defined, although there has been some confusion surrounding the junior synonyms of the species. This was clarified by Bello (2011), and we follow Bello (2011) by including Sepiola petersii (Steenstrup, 1887) and Sepiola scandica Steenstrup, 1887 as junior synonyms of Sepietta oweniana. The nomenclature of Sepiola atlantica is straightforward. The date of the taxon authority was determined from dates of publication of text and plates for Férussac and d’Orbigny’s 1834–1848 monograph (Tillier and Boucher-Rodoni, 1993). Within each species account, we indicate the full classification (systematic) of the species and report the type locality and repository. Remarks on previous misidentifications as well as recent revisions of systematics and relevant results of genetic studies are covered in the following section. We follow the higher taxonomy provided on the Tree of Life (tolweb.org), because this is considered to be the most accurate up-to-date intepretation of cephalopod phylogenetic relationships. Therefore, we do not include “Teuthida”, but treat Myopsida and Oegopsida as separate orders without assuming a sister-taxon relationship between them. Cephalopod biology and fisheries in Europe: II. Species Accounts | 7 Diagnosis We describe how eggs, hatchlings, juveniles, and adults can be identified, providing photographs where appropriate and, where relevant, providing details on differences between similar species. Note that an identification guide to paralarvae of Mediterranean cephalopod species has recently been as a Cooperative Research Report (Zaragoza et al., 2015). Here, we also deal with issues of species status. This is particularly relevant in the case of the two Alloteuthis species, for which recent molecular and morphometric studies have done little to clarify the true taxonomic identity of the two familiar European morphotypes. For a glossary of technical terms used, see the cephalopod pages on the Tree of Life website (http://www.tolweb.org/notes/?note_id=587). Unless otherwise stated, lengths given are dorsal mantle length (ML). Total length (TL) is sometimes reported in the literature, e.g. for hatchlings, and is also indicated herein when relevant. For early life stages and species with small adults, measurements are normally given in millimetres, otherwise in centimetres. Weight data normally refer to total body weight. We have not standardized units throughout, but rather use them as given in original papers. Note that fin length is measured along the anterior–posterior axis, i.e. parallel to the body, and fin width refers to the maximum distance between the distal edges of both fins, measured laterally (perpendicular to the main body axis). In relation to suckers on arms and tentacle clubs, we follow the convention employed by the Tree of Life website in using "series" to refer to longitudinal rows of suckers and “rows” to indicate transverse rows of suckers. Remarks For some species, there remain issues or doubts, e.g. in relation to the taxonomic status of the species, the reliability of diagnostic features, or our knowledge of distribution. These issues are discussed in the Remarks section. Life history This section gives an account of the life cycle. Egg, paralarva, juvenile, and adult stages are described, considering the growth and maturation processes, spawning and fecundity, and the seasonality of these processes and events. Where relevant, we discuss evidence of how environmental conditions or environmental variation affect growth and maturation. For most species, length–weight relationships and length-at-maturity are available. Egg and juvenile development This section summarizes knowledge of early life stages. 8 | ICES Cooperative Research Report No. 325 Growth and lifespan Determination of age is essential to allow determination of lifespan and the time-scale of maturation, and to calculate growth rates. We use age data as reported. However, it should be noted that some caution is needed when interpreting apparent geographic differences in lifespan and growth rates obtained by different authors. For example, there are indications that differences in increment interpretation by different readers may have contributed to the different results reported by Arkhipkin (1995) and Raya et al. (1999) for Loligo vulgaris on the West Saharan shelf. Issues of accuracy and precision are common for age readings based on hard structures in marine animals and are generally addressed through practical workshops and exchange programmes, as for otolith reading in fish species subject to stock assessment. There is a need for regular intercalibration exercises as part of quality assurance for statolith readings (e.g. Jereb et al., 1991). Cephalopod growth is generally described as continuous and non-asymptotic (Jackson and Moltschaniwskyj, 2002), although the growth of several ommastrephid squid species has been modelled using Gompertz or logistic models (which are both asymptotic models), e.g. Arkhipkin et al. (2000), Hendrickson (2004), and Markaida et al. (2004). As pointed out by Forsythe and Van Heukelem (1987), cephalopod growth typically has two phases: an initial rapid growth phase often described as “exponential”, and a second phase of slower growth sometimes called “logarithmic”. During exponential growth, the specific (instantaneous) growth rate is by definition constant. In practice, measured instantaneous growth rates often seem to decline continuously from hatching to maturity (in other words, even if there are two growth phases, the first one is not strictly exponential, and the apparent dichotomy may be more arbitrary than real). Consequently, for growth-rate data to be meaningful, it is essential to report the size (and, if known, the age) of the animals in which it was measured. Growth rates are reported in several different ways in the literature. In some cases, equations are fitted to data on length or weight vs. age. More commonly, growth is reported either as an absolute rate (mm d–1 or g d–1) or as the percentage increase in mantle length or body weight per day (otherwise known as the specific or instantaneous growth rate). Length–weight relationships For all species, we present length–weight relationships within the life history section, and, where possible, provide separate equations for both sexes in each region. Generally, length–weight relationships were originally calculated using simple least-squares regression; although, if some other technique was used, we note this fact. It became apparent in compiling and plotting the curves that the equations presented in many source papers (including several written by authors and editors of this report) contain errors. Having established how the errors arose (e.g. wrong specification of units, misplaced decimal points), we corrected those equations. The use of different units of measurement makes comparisons difficult. Therefore, we present all our data on length–weight relationships as W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). We do not give the equation per se, but rather present the values for the parameters a and b. Standardizing all relationships to weight in grammes and length in centimetres and presenting them in a consistent format allows comparisons to be made easily between sexes and locations. This required some recalculation of parameter values, explained below. Cephalopod biology and fisheries in Europe: II. Species Accounts | 9 Annex 2 contains regression equations used to estimate cephalopod sizes (ML and W) based on measurements of beaks for the 17 species described in this volume. Using ML in cm is logical, because the parameter a falls in a range that is easily presentable (usually between 0.1 and 1, although it varies by location and species). Use of ML (mm) would lead to greater scope for error, especially in species where the parameter a tends to be small, e.g. in Todarodes sagittatus. Off Norway, that species was found to have a relationship between mantle length (cm) and weight (g) defined by the equation W = aMLb, where a = 0.0091 and b = 3.23. This may also be written as W(g) = 0.0091ML(cm)3.23. Of course, it is more common to measure mantle length in mm than in cm. However, if this same relationship is expressed in terms of mm, the parameter a becomes 0.000005342 or 5.342 × 10–6 (the parameter b remains unchanged). Hence, we could also write W(g) = 0.000005342ML(mm) 3.23 or W(g) = 5.342 × 10–6 ML(mm)3.23. All the equations in this paragraph represent an identical length–weight relationship derived from a single dataset. We argue that, expressed in mm, the value of parameter a is more prone to errors (simple mistyping of the number of zeros) and is more difficult to compare (for example, most people find it intuitively difficult to compare a number × 10–6 with one that is × 10–3). A length–weight relationship calculated using ML in mm can be converted to one based on ML in cm as follows. As an example, we use the relationship for T. sagittatus cited in the above paragraph: W(g) = aML(mm)b where a = 0.000005342 and b = 3.23, i.e.: W(g) = 0.000005342 ML(mm)3.23 We can rewrite this as: W(g) = 0.000005342 ML(cm × 10)3.23 Note that the only thing changed so far is that mm has been rewritten as (cm × 10). All we now do is rearrange the equation to remove the ”10” from within the brackets: W(g) = 0.000005342 ML(cm) 3.23 × (10)3.23 W(g) = (0.000005342)x(10)3.23 ML(cm)3.23 W(g) = 0.0091 ML(cm)3.23 In other words, one can simply multiply the value of a, taken from a relationship expressed in mm, by 10b to obtain the value of a for a relationship expressed in cm. Clearly then, to convert from a relationship expressed in cm to a relationship expressed in mm, one simply divides by 10b. In recalculating equations, we have not been able to go back to the original data and rely on simple rearrangement of equations. While this would have facilitated comparison across studies, it is not, strictly speaking, statistically robust. It should be noted that the estimated best fit will have been contingent on the transformation applied to the data (and hence, implicitly, the statistical distribution of weight-at-length) as well as the fitting procedure. Most studies applied simple linear regression to log-transformed data (implying a lognormal distribution of weight at length and increasing variance in weight at higher length values) despite the fact that this will introduce bias for at least two reasons. First, given that neither length nor weight measurements are error-free, use of orthogonal regression is more appropriate. Second, the mean of a set of log-normally distributed Y values is not the same as the expected Y derived from the straight line fitted to log- 10 | ICES Cooperative Research Report No. 325 transformed values. This bias in expected Y is usually ignored, but, as noted by Beauchamp and Olson (1973) and Hammond and Rothery (1996), can be corrected by multiplying each weight estimate by ev/2 [or 10v/2.loge(10) if using base-10 logarithms]—where v is the variance about the relevant regression line (see Pierce et al., 2007). We deliberately avoid using the term “allometry” in relation to the slope coefficient (normally represented as “b”) of the length–weight relationship. Weight is not a linear measurement, so we argue that length–weight relationships do not express allometry or isometry in the usually intended sense of different body parts growing at different or similar rates. The slope coefficient departs from 3.0 to the extent that cephalopods are not spherical, which is to say usually to a considerable degree (excluding the possibility that average tissue density changes directionally as the animal grows in size). Maturation and reproduction We give length-, weight-, and/or age-at-50% maturity values (MLm50%, BWm50%, age m50%) where available, basing our notation on that used by Silva et al. (2004). These values are usually given separately for males and females and are obtained by fitting a logistic regression to maturity and size or age data. However, some authors also quote the size at which (say) 75% of animals are mature or the size at which all animals are mature. Additional related terms include “size at first maturity”, presumably in the sense of the smallest size at which an animal can mature (MLmmin) or, in practical terms, the smallest mature animal identified. Finally, some authors refer to “mean size at maturity”. This sounds as though it should refer to the average of the sizes at which individuals reach maturity, but such information is unlikely to be available, and the term is presumably normally used to indicate the mean size of mature animals. A few references give comprehensive information on the smallest size at maturity, size at 50% maturity, and the size at which all animals are mature. Another possible source of confusion relates to the maturity scale used and the stage which is regarded as mature. Stage IV is normally used as an indication of maturity, and stage V represents animals in the process of spawning or releasing spermatophores (although in the case of males, the difference between stages IV and V may be an artefact of handling, with post-mortem mechanical pressure forcing spermatophores into the penis). Most cephalopod maturity scales are ultimately based on Lipiński (1979), but the concept has recently been revisited in an ICES-sponsored workshop (ICES, 2010). In loliginids, the existence of at least two growth forms (presumed to be associated with different reproductive strategies) in males results in (at least) two size modes at maturity and, consequently, MLm50% values are meaningful only if these modes can be separated in the analysis. The different growth forms may be evident as different size modes in length-frequency distributions. Where these size modes can be followed through time, and especially where they can be linked to distinct hatching periods, it is usual to speak of the existence of two or more “microcohorts”. Use of the unmodified term “cohort” is misleading because it normally refers to animals hatched/born in the same year; under this definition, different cohorts of squid probably coexist only for a very short period (if at all), although two cohorts can be present in cuttlefish. As the different hatching periods are usually within the same year and/or separated by only a few months at most, the term “microcohort” is more appropriate. Because the terminology is now widely used, we follow Rocha et al. (2001) in describing spawning strategies (e.g. intermittent terminal spawner, multiple spawner). Part of the Cephalopod biology and fisheries in Europe: II. Species Accounts | 11 rationale for the development of this terminology was the original definition of iteroparous organisms (Cole, 1954) as those with more than one reproductive event in their lifetime, whereas semelparous organisms reproduce only once, a definition under which it is difficult to decide whether most coleoid cephalopods should be called semelparous or iteroparous. However, iteroparity is more commonly understood to imply the occurrence of resting phases, during which gonads become inactive, between spawning events. Under this definition, it is clear that most if not all coleioid reproductive strategies represent variants of semelparity. Neverthless, the categories of Rocha et al. (2001) offer a useful way of classifying these strategies. Natural mortality We include a brief section on natural mortality where this information is available. Because of the widely differing life histories (particularly with respect to early life stages), the temporal distribution of natural mortality events can vary greatly between species. Biological distribution The environmental characteristics of the species’ ranges are described, including the usual ranges of bathymetry, temperature [e.g. sea surface temperature (SST)], salinity, substratum. We generally give salinity without units, although in cases where it would be otherwise unclear, we use the notation “psu” (practical salinity unit). Where information is available, habitat requirements at particular life stages or for particular activities (e.g. spawning) are described, as are the effects of variation in environmental conditions on distribution and abundance. Such inferences are usually drawn from empirical statistical modelling or experiments in captivity. Finally, this section describes horizontal and vertical migrations. Trophic ecology Our knowledge of prey and predators for each species is summarized, and tables are provided with lists of prey and predator species. In the tables, we excluded predation on paralarvae and eggs, not least because it is poorly documented, and we also exclude cannibalism, although its occurrence is covered in the text. Topics such as ontogenetic, seasonal, and environmental variation in diet composition are also discussed. Other aspects of ecology Where available, this may include information on parasites, contaminant bioaccumulation, and other topics that do not obviously fall under the heading of distributional and trophic ecology. Other topics covered include aspects of population dynamics and abundance fluctuations. Fisheries and aquaculture The fisheries section includes information on recruitment, because it is the life cycle process that most directly influences fishery catches. It also describes the nature and current status of the fisheries. Updating information published in the previous CRR (Pierce et al., 2010), it briefly reviews which countries catch what species, the fleets and gears involved, the importance of the capture fisheries in terms of landings and effort, and any trends in landings. We also briefly mention what is known of population structuring in these species and, specifically, how many stocks or management units exist. Where they exist, we describe any current stock assessment and fishery management. 12 | ICES Cooperative Research Report No. 325 Throughout this section, we assume familiarity with the FAO term ”nei”, an abbreviation for “not elsewhere included” and used as a recording category in fisheries statistics for groups of species that are not listed individually. Where relevant, the current status of aquaculture development is described. Future research needs, bibliography, and illustrations We wanted to identify gaps that should be addressed in future research, especially relative to future fishery exploitation, assessment, and management. The bibliography is in two parts: literature cited in the review, which is subsumed within the general bibliography; and additional relevant publications for each species. Each account is accompanied by photographs, line drawings, and graphic presentations of data. These usually include a photograph and a line drawing of the species at the beginning of each account. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Octopus vulgaris Common octopus | 13 14 | 3 ICES Cooperative Research Report No. 325 Octopus vulgaris Cuvier, 1797 Pilar Sánchez, Roger Villanueva, Patrizia Jereb, Ángel Guerra, Angel F. González, Ignacio Sobrino, Eduardo Balguerias, João Pereira, Ana Moreno, A. Louise Allcock, Evgenia Lefkaditou, Graham J. Pierce, José Iglesias, and Uwe Piatkowski Common names Pieuvre, poulpe (France) ; Χταπόδι [chtapodi] (Greece) ; polpo (Italy) ; polvo (Portugal) ; pulpo común (Spain) ; common octopus (UK) (Figure 3.1). Synonyms (Following Norman and Hochberg, 2005). Octopus albus Rafinesque, 1814: 29, Octopus heteropus Rafinesque, 1814: 28, OctoFigure 3.1. Octopus vulgaris. Dorsal view. From Guerra (1992). pus maculatus Rafinesque, 1814: 29, Octopus moschatus Rafinesque, 1814: 28, Octopus niger Rafinesque, 1814: 28, Octopus ruber Rafinesque, 1814: 28, Octopus brevitentaculatus Blainville, 1826: 187, Octopus tetradynamus Rafinesque, 1814: 28, Octopus pilosus Risso, 1826: 4, Octopus cassiopeia Gray, 1849: 9, Octopus bitentaculatus Risso, 1854: 61, Octopus rabassin Risso, 1854: 67, Octopus tritentaculatus Risso, 1854: 63, Octopus troscheli Targioni-Tozzetti, 1869: 156, Octopus octopodia Tryon, 1879: 113, Octopus coerulescentes Arbanisch (Fra Piero), 1895: 267. 3.1 Geographic distribution The common octopus, Octopus vulgaris Cuvier, 1797, is found in the Northeast Atlantic and the Mediterranean (Figure 3.2), and its presence is also reported in the western Atlantic (Caribbean Sea and northern South America), South Africa, India, and East Asia (Norman et al., 2014; see Remarks section below). In the Northeast Atlantic, it extends from Dublin and Liverpool Bay (Massy, 1928), along the southern British coasts (Rees, 1950), occasionally as far as the southern North Sea (Grimpe, 1925; Adam, 1933; Jaeckel, 1958). Common along the French, Spanish, and Portuguese coasts (Magaz, 1934; Bouxin and Legendre, 1936; Sousa Reis, 1985), it is especially abundant on the Sahara Bank, off West Africa between 26 and 19°N (Bas, 1975; Bravo de Laguna, 1989), extending farther south and west to the Cape Verde Islands (Adam, 1962), and as far as the equator (Adam, 1983). Very abundant in the Azores region (e.g. Gonçalves, 1991), it is recorded from Madeira (Rees and Maul, 1956) and the Canary Islands (Hernández-García et al., 1998a, 2002). It is widely distributed and abundant throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello 2004; Salman, 2009), including the western and central Mediterranean (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Lefkaditou et al., 2003a), and the Aegean Sea and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak et al., 2008). Old records of the Cephalopod biology and fisheries in Europe: II. Species Accounts | 15 species in the Sea of Marmara exist (e.g. Demir, 1952, in Ünsal et al., 1999), but Octopus vulgaris has not been recorded by more recent research carried out in those waters (Katagan et al., 1993; Ünsal et al., 1999). Figure 3.2. Octopus vulgaris. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 3.2 Taxonomy 3.2.1 Systematics Coleoidea – Octopodiformes – Octopoda – Octopodidae – Octopus. 3.2.2 Type locality Not stated in the original description of Cuvier (1797) but presumed to be western Mediterranean Sea. 3.2.3 Type repository No type is believed to exist (see Lu et al., 1995). 3.3 Diagnosis 3.3.1 Paralarvae At hatching, paralarvae have an elongate, conical mantle. They are 2–3 mm long (total length). The arms are subequal in length, with three suckers on each arm and two chromatophores in one row on each arm. Hatchlings from the Northwest Pacific have 3–4 suckers per arm (Villanueva and Norman, 2008). See Hochberg et al. (1992) for a description of the full chromatophore pattern (but see also Figure 3.3 below). 16 | ICES Cooperative Research Report No. 325 Figure 3.3. Octopus vulgaris. Individuals from hatching to settlement obtained from rearing experiments described in Villanueva (1995a). Images not to scale. Age (d) and mantle length (ML) of the individuals measured fresh are: (A) 0 d, 2.0 mm ML; (B) 20 d, 3.0 mm ML; (C) 30 d, 4.3 mm ML; (D) 42 d, 5.9 mm ML; (E) 50 d, 6.6 mm ML; and (F) 60 d, 8.5 mm ML. Octopuses from this experiment settled between 47 and 54 d. Individuals were photographed under anaesthesia (2% ethanol) potentially causing chromatophore contraction in some cases. Photos: Jean Lecomte, modified from Villanueva et al. (1995). 3.3.2 Juveniles and adults Adults reach 40 cm ML and 140 cm total length. They have a muscular sac-shaped mantle with a wide pallial aperture that extends beyond its lateral edges. The arms are robust at the base: the lateral arms are longest, and the dorsal ones shortest. The arms have two series (i.e. longitudinal rows) of suckers. Suckers 15–17 of arms 2 and 3 are enlarged in adults, especially in males. The third right arm of mature males is hectocotylized. The ligula is short and spoon-shaped. There are 7–11 lamellae on the outer side of the gill, including terminal lamellae. There are four papillae in the dorsal part of the mantle (one situated in the anterior part, another posterior, and two laterals). The species has reticulated skin, with four whitish spots: two between the eyes and two below the first dorsal papilla. The lower mandible (beak) is illustrated in Figure 3.4 (see also Nixon, 1969, and Clarke, 1986). Cephalopod biology and fisheries in Europe: II. Species Accounts | 17 Figure 3.4. Octopus vulgaris. Lower beak (left) and upper beak (right), lateral views. Photo: Evgenia Lefkaditou. 3.4 Remarks Octopus vulgaris was traditionally believed to be a cosmopolitan species with a worldwide distribution (Roper et al., 1984). Mangold and Hochberg (1991) and Mangold (1998) redefined its boundaries, suggesting that its distribution was restricted to the Mediterranean and the eastern Atlantic. Subsequent molecular work using the mitochondrial markers 16S rRNA and COIII showed, however, that the distribution of O. vulgaris in the Atlantic apparently extends to southern Brazil (Söller et al., 2000) in the west, to Lanzarote and Senegal in the east, and as far south as Tristan de Cunha and False Bay, South Africa (Oosthuizen et al., 2004; Warnke et al., 2004; Teske et al., 2007), and that it is also in the Indian Ocean (Guerra et al., 2010a). Samples from Japan and Taiwan in the Pacific also appear to be conspecific with O. vulgaris. Nonetheless, those studies also showed that, throughout this distribution, there are octopuses that have been previously attributed to O. vulgaris that are, in fact, distinct species, e.g. Octopus insularis recently described from Brazil (Leite et al., 2008). Substantial differences between the chromatophore patterns of paralarvae from the eastern and western Atlantic have been observed, which could provide evidence for the existence of distinct populations or even cryptic O. vulgaris-like species along the southern Brazilian coast (Vidal et al., 2010). See Fioroni (1970), Packard (1974), and Messenger (2001), among others, for accounts of chromatophores in O. vulgaris. According to Norman et al. (2014), the name Octopus vulgaris is currently applied to at least five morphologically similar, but unresolved, taxa with disjunct distributions across subtropical and temperate waters worldwide: Octopus vulgaris sensu stricto Mediterranean Sea, Central and Northeast Atlantic Octopus “vulgaris” type I Tropical western Central Atlantic Octopus “vulgaris” type II Subtropical Southwest Atlantic: Brazil Octopus “vulgaris” type III Temperate South Africa and southern Indian Ocean Octopus “vulgaris” type IV Subtropical/temperate East Asia All are of high profile and have high fisheries value. All forms produce small eggs with planktonic hatchlings capable of wide dispersal across the open ocean, potentially supporting gene flow between the disjunct distributions of at least some forms. The species complex is in urgent need of revision and is highly likely to contain cryptic species (Norman et al., 2014). Clearly, the true range of O. vulgaris has not yet been elucidated; however, its distribution throughout the Mediterranean and eastern Atlantic is undisputed. 18 | 3.5 ICES Cooperative Research Report No. 325 Life history The life history of the species is annual, with spawning year-round but with peaks in spring and autumn. 3.5.1 Egg and juvenile development The early part of the life cycle of this species is reviewed by Mangold and Nixon (1996). The duration of the egg stage depends on incubation temperature, ranging from 20–30 d at 25°C to 100–120 d at 13°C (Mangold, 1983a). Under laboratory conditions, the duration of the planktonic phase seems to be inversely related to rearing temperature, ranging from 33 d at 25°C to nearly 2 months at 21°C. Recently, benthic juveniles of 8– 10 mm ML have been found with 23–25 suckers per arm and weighing 100–125 mg fresh weight. Subadults reach 0.5–0.6 kg by 6 months after hatching in the laboratory (Itami et al., 1963; Imamura, 1990; Villanueva, 1995a; Iglesias et al., 2004; Okumura et al., 2005; Carrasco et al., 2006). Moreno et al. (2009) found octopus paralarvae in plankton samples from Portuguese coastal waters (from 57 surveys during the period 1986–2004) mainly in the second half of the year, with peaks in July and November, probably related to two seasonal spawning peaks in Portuguese waters. Those authors also report a relationship between paralarva abundance and favourable upwelling conditions. In Galicia, seasonal upwelling is in late summer and early winter, and the (single) peak in hatchling abundance coincides with maximum zooplankton abundance (Otero et al., 2007). 3.5.2 Growth and lifespan The life cycle (embryonic and post-hatching life) has been completed under laboratory conditions, resulting in a lifespan of 356 and 339 d for a female and a male of 1.8 and 1.6 kg at death, respectively, reared with food in excess and in temperatures of 17–23°C (Iglesias et al., 2004). Sánchez and Obarti (1993) reported a maximum age of 15 months in the Mediterranean. Katsanevakis and Verriopoulos (2006) estimated a lifespan of 12–15 months in the eastern Mediterranean using a time-variant, stage-classified, matrix population model based on monthly density measurements of four size stages (1, <50g; 2, 50–200 g; 3, 200–500 g; and 4, >500 g) recorded during scuba diving. Perales Raya (2001) estimated the maximum age of O. vulgaris to be 12 months in Sahara Bank populations based on beak growth increment counts, and Hernández-López et al. (2001) estimated the maximum ages of males and females to be 12.3 and 13.3 months, respectively, in Canary Island populations. Smale and Buchan (1981) reported a maximum age of 12 months for females and 15 months for males under culture conditions off the east coast of South Africa, whereas Domain et al. (2000) reported lifespans of 14–17 months for females and 18–20 months for males in Senegalese waters. Daily increment deposition in O. vulgaris stylets has been validated in individuals maintained in aquaria and ranging in size from 248 to 1470 g (Hermosilla et al., 2010). Octopus vulgaris is characterized by rapid non-asymptotic growth (Alford and Jackson, 1993), with great individual variability in increases in length or weight. This variability has been found both in culture (Iglesias et al., 2004) and in the wild (Domain et al., 2000). Growth rate is influenced mainly by diet (Forsythe and van Heukelem, 1987; García García and Cerezo Valverde, 2006; Cerezo Valverde et al., 2008) and temperature (Aguado Giménez and García García, 2002), although several authors have noted extreme variation in growth, even among individuals reared at the same temperature Cephalopod biology and fisheries in Europe: II. Species Accounts | 19 and fed the same food (Forsythe and van Heukelem, 1987; Villanueva, 1995a; Semmens et al., 2004). As in most if not all cephalopods, instantaneous relative growth rates (i.e. % increase in BW d–1, or, sometimes % increase in ML d–1) decrease in older animals, values ranging from 6.14 (%BW d–1) in the smallest individuals to 0.94 in the largest (Forsythe and van Heukelem, 1987). Villanueva (1995a) measured daily growth rates of 2.49% ML d – 1 and 8.19% BW d –1 during the first 2 months of life. Growth rates, usually for large animals, have been measured in captivity by a number of authors. Mangold and Boletzky (1973) recorded growth rates at temperatures between 10 and 20°C. Although they noted great variation between individuals, daily growth rate was generally faster at higher temperatures. At 20°C, daily growth ranged from 1.68 to 4.14% of BW, although it reached 5% over short periods. This compares with 1.50–1.91% (2.74%) at 15°C and 0.78–1.01% (1.57%) at 10°C. Pham and Isidro (2009) obtained growth rates of 0.67–1.47% of BW d–1. Estefanell et al. (2013) recorded growth rates of 1.6–1.8% of BW d–1 in captivity. Captive and wild growth rates were measured by Domain et al. (2000), the former based on tagging animals off Senegal, in waters of >20°C. Growth was slower in males than in females. The growth rate was ca. 1.36% of BW d–1 (both sexes combined) in captivity and between 0.85 (males in 1997) and 1.51% (females in 1998) in the wild, with slower growth at temperatures >25°C. Length–weight relationships are summarized in Table 3.1. Table 3.1. Octopus vulgaris. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations are converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Galicia 0.442 2.918 F Guerra (1981) 0.296 3.029 M 0.365 2.961 All 2.9 2.17 All Otero et al. (2007) 3.277 2.267 F Silva et al. (2002) 2.489 2.369 M 2.895 2.313 All 0.587 2.83 F 0.758 2.74 M 0.626 2.8 All 0.542 2.804 F Gulf of Cádiz South Africa Northwestern Mediterranean Sea Smale and Buchan (1981) Guerra and Manriquez (1980) 0.350 2.988 M 0.420 2.917 All 0.413 2.916 F 0.442 2.882 M 0.437 2.889 All 1.654 2.576 F 3.306 2.323 M Gulf of Alicante 0.51 2.87 All González et al. (2011) Tunisia 0.371 2.8335 F Jabeur et al. (2012) 0.485 2.834 M Balearic Islands Catalan Sea Quetglas et al. (1998a) Sánchez and Obarti (1993) 20 | ICES Cooperative Research Report No. 325 0.399 2.915 All Aegean Sea 0.138 2.60 All Lefkaditou et al. (2007) Northeastern Levant Sea 0.031 3.841 F Duysak et al. (2008) 0.1685 3.1219 M 0.1399 3.2001 All 3.5.3 Maturation and reproduction In Galicia, the sex ratio is ca. 1:1 most of the year, although females dominate samples collected in May (1:0.73) and September (1:0.58) (Otero et al., 2007). Quetglas et al. (1998a) recorded the sex ratio in the Balearic Sea (Mediterranean) for each season and found no significant differences from 1:1. In the Gulf of Cádiz, the annual sex ratio was estimated as 1.06:1 (male:female) (Silva et al., 2002). However, Smale and Buchan (1981) reported that, off South Africa, male numbers dominated during the months March– September and females during October–February (with the greatest departure from 1:1 in November when the sex ratio was ca. 3:1 in favour of females). Females mature larger than males (Lourenço et al., 2011a, b). In Galicia, weight at 50% maturity (BWm50%) was 1788 g for females and 903 g for males. The smallest mature females were 12 cm ML and 394 g BW, and the smallest mature males were 10 cm ML and 323 g BW (Otero et al., 2007). In the Gulf of Cádiz, lengths (ML) and weights (BW) of the smallest mature specimens sampled by Silva et al. (2002) were 9.4 cm and 250 g in males, and 12 cm and 580 g in females. Length at maturity (MLm50%) was 10.4 cm ML in males and 17.6 cm ML in females, and BWm50% was estimated at 671 g in males and 2023 g in females. In the western Mediterranean, mantle length at first maturity is ca. 9.5 cm in males and 13.5 cm in females (Mangold-Wirz, 1963a). Cuccu et al. (2013) reported that the smallest mature specimens sampled in Sardinian waters (central western Mediterranean Sea) were 45 mm ML and 190 g BW in males, and 90 mm ML and 310 g BW in females. The MLm50% was 70 mm for males and 120 mm for females, and BWm50% was 320 g and 520 g for males and females, respectively. Males matured at 170–470 d, younger than females (210–390 d). The spawning season extends throughout the year, with two peaks: one in spring and one in autumn in Northeast Atlantic populations. The main spawning season in the Mediterranean is June–July (Mangold, 1997). Rees and Lumby (1954) refer to spawning beginning in May in the English Channel, the precise timing varying with location and, possibly, temperature. In Galician waters, maturity and reproductive indices indicated spring to be the most important spawning season, although mature females are present during the months December–August, with a peak in May that is related to seasonal upwelling (Otero et al., 2007). In northwestern Portugal, the species spawns during the period March–July, again coinciding with the northwest coast upwelling season, whereas on the south coast of Portugal, the species spawns mainly in summer between August and September, although there is sometimes a minor spawning peak in early spring along the south coast (Lourenço et al., 2011a). In the Gulf of Cádiz, the breeding season extends from February to October, with spawning peaks in April–May and August (Silva et al., 2002). In the Gulf of Alicante, the gonadosomatic index peaks between April and July for males and in July for females (González et al., 2011). The potential fecundity of mature females ranges from 70 000 to 634 445 oocytes (Mangold-Wirz, 1963a; Silva et al., 2002; Otero et al., 2007). Females attach small oval eggs of ca. 2.5 × 1 mm (Mangold-Wirz, 1963a) to hard substrata, mainly rocks, and care for the eggs until hatching. Cephalopod biology and fisheries in Europe: II. Species Accounts | 21 The maximum number of spermatophores observed in the Needham’s sac is 633 (Otero et al., 2007), and the number and length of spermatophores tends to increase with size of male. In Galician waters (northwestern Spain), mean (± s.d.) potential fecundity was estimated at 221 447 ± 116 031 oocytes and mean oocyte length at 3.0 ± 0.8 mm. The mean number of fully developed spermatophores was 182 ± 88, with a mean length of 48.8 ± 10.6 mm (Otero et al., 2007). 3.5.4 Natural mortality The natural mortality of cephalopods during paralarva and settlement stages is high and is strongly related to environmental factors, which ultimately control the abundance of food for the paralarvae (zooplankton). The link between upwelling episodes and subsequent fishery catch rates for octopuses in Galicia is consistent with environmental factors having a major impact during the pelagic stage of the life cycle (Otero et al., 2008). In the eastern Mediterranean, more than 50% of just-settled individuals die within three months, and the mortality rate falls thereafter up to ca. 6 months after settlement (Katsanevakis and Verriopoulos, 2006). 3.6 Biological distribution 3.6.1 Habitat Octopus vulgaris is a merobenthic species inhabiting temperate, tropical, and subtropical waters. It is found from the coast out to the outer edge of the continental shelf (200 m) in temperatures of 6–33°C. Rees and Lumby (1954) note that the species tolerates temperatures as low as 6°C in the English Channel. It is a stenohaline species, tolerating salinity ranging from 29 (Delgado et al., 2011) to 40 (Mangold, 1983a). Local density of O. vulgaris, as has been documented for other species of octopuses, is affected by the availability of solid material (rocks, stones, shells, anthropogenic litter, etc) to be utilized for den construction (Katsanevakis and Verriopoulos, 2004). 3.6.2 Migrations This species undertakes limited seasonal migrations. According to Rees and Lumby (1954), octopuses appear to move away from inshore waters in late summer and spend winter in deeper, offshore waters. No segregation between sexes has been observed (Mangold, 1983a). 3.7 Trophic ecology 3.7.1 Prey The diet of O. vulgaris consists of crustaceans, fish, molluscs, and polychaetes (Table 3.2). No significant variation in diet has been reported for subadults and adults. Anraku et al. (2005) showed that prey selection under experimental conditions depended on chemical stimuli detected by chemoreceptors in the arms and lip (see Graziadei, 1971, for a description of the nervous system of the arms). Octopuses drill holes in the shells of shelled molluscs, allowing them to inject cephalotoxin, secreted by the posterior salivary glands, to paralyse the prey (e.g. Ghiretti, 1959, 1960; Cariello and Zanetti, 1977; Nixon, 1979; Nixon et al., 1980). Table 3.2. Prey composition of Octopus vulgaris, as known from studies in the Mediterranean Sea, Northeast Atlantic, and Sahara Bank (compiled from Nigmatullin and Ostapenko, 19761; Guerra, 19782; Ambrose and Nelson, 19833; Nixon and Budelmann, 19844; Sánchez and Obarti 19935; Quetglas et al. 1998a6; Kallianiotis et al., 20017; Roura et al., 20128; Á. Guerra, pers. comm.9) 22 | ICES Cooperative Research Report No. 325 Taxon Species Osteichthyes indet.6,8 Blenniidae Blennius ocellaris (butterfly blenny)6, indet.9 Caproidae Capros aper (boarfish)6 Carangidae Decapterus spp.1, Trachurus spp.1 Carapidae Carapus acus (pearl fish)6 Centracanthi- Centracanthus cirrus (curled picarel)6 dae Cepolidae Cepola macrophthalma (as C. rubescens) (red bandfish)2,7 Clupeidae Sardinella spp.1, indet.2 Congridae Conger conger (European conger)7 Gobidae Gobius niger (black goby)7, indet.9 Labriidae indet.9 Lotidae Gaidropsarus vulgaris (three-bearded rockling)6 Ophichthidae Ophichthus rufus (Rufus snake-eel)6, Leptocephalus spp.1 Ophidiidae Ophidion barbatum (snake blenny)7 Serranidae indet.9 Soleidae indet.1 Sparidae Boops boops (bogue)1, Dentex macrophthalmus (large-eye dentex)1, Dentex gibbosus (pink dentex)1, Dentex spp.1, Pagellus acarne (auxilliary seabream)1, Pagellus erythrinus (common pandora)1 Trachinidae Trachinus spp.1 Triglidae indet.1,9 Uranoscopidae Uranoscopus spp.2 Chondrichthyes Scyliorhinidae Scyliorhinus canicula (lesser spotted dogfish)7 Crustacea Decapoda Dendrobranchi- indet.6 Melicertus kerathurus2, Solenocera membranacea2 ata-Penaeiodea PleocyemataAnomura Anapagurus laevis2, Anapagurus spp.2,5, Galathea bolivari6, G. intermedia6, G. strigosa6, Galathea spp.2,6, Paguristes eremita6, Pagurus prideaux6, Paguridea indet.6, Pisidia longicornis2, Pisidia spp.5, indet.8 Pleocyemata- Atelecyclus rotundatus6, Atelecyclus spp.9, Calappa granulata2, Brachyura Cancer pagurus9, Carcinus maenas9, C. aestuarii (as C. mediterraneus)2, Dromia personata2, Ebalia granulosa6, E. tuberculosa6, Ebalia spp.6, Eriphia verrucosa9, Ethusa mascarone2, Eurynome spinosa6, Goneplax rhomboides2,5,7, Inachus dorsettensis6, Inachus spp.2,9, Liocarcinus corrugatus2,6, L. depurator2,5,7, L. pusillus6, L. vernalis5, Liocarcinus spp.2,6,9, Macropodia spp.9, Maja squinado9, Medorippe lanata2, Necora puber (as L. puber)9, Pachygrapsus marmoratus9. Pachygrapsus spp.2, Parthenopidae indet. 6, Pilumnus spinifer6, Pisa armata2, P. nodipes2, Polybius henslowii9, Xantho pilipes6,8, indet.5,6,8 Pleocyemata- Aegaeon cataphracta (as Pontocaris cataphracta)2,5, Alpheus Caridea spp.2,5, Alpheidae indet.6, Crangon crangon2, Eualus cranchii (as Thoralus cranchii)6, Palaemon serratus5, Palaemon spp.2,9, Pandalina brevirostris2, Philocheras sculptus6, Philocheras spp.2, Processa spp.2, indet.6,8 Cephalopod biology and fisheries in Europe: II. Species Accounts Pleocyemata- | 23 indet.8 Thalassinidea Stomatopoda Unipeltata-Squil- indet.1 Squilla mantis2 loidea Euphausiacea indet.8 Amphipoda indet.1,2 Gammaridea indet.6 Ostracoda indet.1 Peracarida-Isopoda indet.1,6 Cephalopoda indet. 6 Myopsida Alloteuthis africana1, A. media6, Loligo vulgaris1,2,6 Octopoda Eledone moschata7, Octopus vulgaris5,9, Octopus spp.1,2 Sepioidea Sepia spp.1,2,5,9, Sepiolidae indet.6 Gastropoda indet.5,7 Cerithioidea Cerithium vulgatum3, Turritella communis6 Conoidea Raphitoma reticulata6 Haliotidea Haliotis tuberculata3 Muricoidea Cymbium spp.1 Naticoidea Naticarius hebraeus6, N. intricatoides6 Patelloidea Patella caerulea3, P. vulgata3 Trochoidea Calliostoma granulatum (granulated top shell)6 , indet.6 Bivalvia indet.1,5,7 Arcoida Arca noae3, Barbatia barbata3, Glycymeris glycymeris3 Pectinoida- Anomia ephippium3 Anomioidea Limoida Limaria tuberculata3 Mytiloida Modiolus barbatus3, Mytilus galloprovincialis9, Mytilus spp.3 Euheterodonta- Ensis ensis9 Solenoidea Veneroida Acanthocardia tuberculata3, Callista chione (as Pitaria chione)3, Cardium spp.3, Chamelea gallina3, Donax semistriatus3, Timoclea ovata3, Venerupis geographica3, Venus verrucosa3 Echinodermata Ophiuroidea indet.1,5 Polychaeta Laetmonice hystrix (as Hermione hystrix)4, indet.1,5 Foraminifera indet.1 3.7.2 Predators Coastal fish (Epinephelus marginatus, Serranus sp., Atherina presbyter) attracted to O. vulgaris egg masses during hatching periods have been observed preying on paralarvae (Villanueva and Norman, 2008). Further, paralarvae of 6.5–18 mm TL have been recorded in the stomach contents of albacore (Thunnus alalunga) (Bouxin and Legendre, 1936). 24 | ICES Cooperative Research Report No. 325 Predators of subadult and adult O. vulgaris include fish, marine mammals, birds, man, and other cephalopod species (Hanlon and Messenger, 1996). Octopus vulgaris has been found in the stomachs of bottlenose dolphin (Tursiops truncatus) (Blanco et al., 2001), Risso’s dolphin (Grampus griseus) (Blanco et al., 2006), and Mediterranean monk seal (Monachus monachus) (Pierce et al., 2011) in the Mediterranean Sea. Marine mammal predators of O. vulgaris in Galician waters include common dolphin (Delphinus delphis), long-finned pilot whale (Globicephala melas), and sperm whale (Physeter macrocephalus) (Table 3.3, see also at González et al., 1994a; López, 2002; Santos et al., 2004a, 2013, 2014). Table 3.3. Known predators of Octopus vulgaris in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopoda Common cuttlefish (Sepia offici- Alves et al. (2006) nalis) Chondrich- Veined squid (Loligo forbesii) Rocha et al. (1994) Bull ray (Pteromylaeus bovinus) Capapé (1977) Smooth-hound (Mustelus mus- Saïdi et al. (2009) thyes telus) Osteichthyes Dusky grouper (Epinephelus mar- Reñones et al. (2002) ginatus) Silver-cheeked toadfish (Lago- Kalogirou (2011) cephalus sceleratus) Pinnipedia Mediterranean monk seal (Mona- Pierce et al. (2011) chus monachus) Cetacea Bottlenose dolphin (Tursiops trun- González et al. (1994a), Blanco et al. catus) (2001), Santos et al. (2007) Common dolphin (Delphinus del- González et al. (1994a), Santos et al. phis) (2004a, 2013) Harbour porpoise (Phocoena Santos et al. (2004b) phocoena) Long-finned pilot whale (Globi- González et al. (1994a), López cephala melas) (2002), Santos et al. (2014) Risso’s dolphin (Grampus griseus) López (2002), Blanco et al. (2006), Bearzi et al. (2011) Striped dolphin (Stenella coerule- Sollmann (2011) oalba) Sperm whale (Physeter macro- González et al. (1994a) cephalus) 3.8 Other ecological aspects 3.8.1 Parasites Hochberg (1983) noted that O. vulgaris was one of only two species in which parasites had been studied in detail. In the genus Octopus, parasites identified included viruses, fungi, sporozoans, ciliates, dicyemids, digeneans, cestodes, hirudineans, and copepods. He noted that two species of the protist Aggregata are known in O. vulgaris: Aggregata octopiana, reported by Schneider (1875), and A. spinosa, described by Moroff (1906). Ciliates found in O. vulgaris include Chromidina coronata. Cephalopod biology and fisheries in Europe: II. Species Accounts | 25 González et al. (2003) recorded a range of parasite species in O. vulgaris from Galicia (more than half of which were also found in Eledone cirrhosa): Aggregata octopiana, which, according to Gestal et al. (2007), is a dangerous pathogen in cultured octopus; Dicyema typus (a mesozoan); Lecithochirium sp. (a digenean trematode); Phyllobothrium sp. and Scolex pleuronectis (both cestodes); Pennella sp. (a copepod); Octopicola superbus (Maxillopoda); and two genera of nematode, Cystidicola sp. and Anisakis simplex sensu stricto. 3.8.2 Contaminants As O. vulgaris is an important fishery resource, the propensity of cephalopods to accumulate certain metals, notably cadmium, is relevant to human health. Seixas et al. (2005a) reported mercury levels from octopuses on the Atlantic coast of Portugal. As expected, the greatest concentrations were in the digestive gland. Although mercury concentrations were slightly higher in samples from Cascais (near Lisbon) than in Viana do Castelo, consistent with the higher concentrations recorded in seawater at Cascais, they were within the range of values legally defined as safe for human consumption. However, cadmium concentrations were above the legal limit for human consumption in samples from Viana in 2002, and two animals also had lead concentrations that exceeded legal limits (Seixas et al., 2005b). In another study based in Portugal, Raimundo et al. (2004) found that cadmium concentrations were greatest in octopuses from the north of the country. Storelli et al. (2012) measured lead, mercury, and cadmium levels in a range of seafood products in Italy (sources from both within and outside Europe), and found the greatest cadmium concentrations in cuttlefish and octopuses, noting that some of the values were close to the legal limits for human consumption. The highest cadmium concentration recorded in O. vulgaris was 0.64 mg g–1 wet weight. 3.8.3 Environmental effects Although the biology and ecology of adult O. vulgaris are generally well documented, there are only a few studies on the effect of physical oceanography on the life cycle of the species. The first such studies were made in waters off Great Britain involving the influence of sea surface temperatures on the reproduction and abundance of adults and the effects of currents on their distribution (Rees, 1950; Rees and Lumby, 1954). Garstang (1900) had previously speculated that a “plague” of octopuses in the English Channel at the end of the 19th century was related to warm summers and mild winters, but, considering subsequent “plague” years, Rees and Lumby (1954) concluded there was no close association between high abundance and warm summers. In the Gulf of Cádiz (southern Iberian Peninsula), a negative correlation was found between rain and abundance (Sobrino et al., 2002). Off Tunisia, there is a strong association between low sea surface temperature and abundance, and in the hot season, rainfall also has a positive effect on production (Chédia et al., 2010). Strong upwelling conditions, interpreted from satellite images, have been related to strong recruitment of O. vulgaris in Mauritanian waters (Faure et al., 2000). In coastal upwelling areas off West Africa, catches of adult O. vulgaris during summer are significantly correlated with the upwelling intensity during the previous winter, indicating the influence of oceanographic conditions on octopus paralarvae and juveniles and the subsequent effects on the fished adult populations (Caverivière and Demarcq, 2002). In the same region, exceptional oceanographic conditions favouring the survival of paralarvae and juveniles also seem to be the origin of demographic explosions of O. vulgaris (Caverivière, 1990; Diallo et al., 2002). A similar relationship between upwelling intensity and adult catches has been found. On the northwestern Iberian coast (Otero et al., 2008), wind stress structure 26 | ICES Cooperative Research Report No. 325 (which is related to upwelling) during spring–summer (prior to the hatching peak) and autumn–winter (during the planktonic stage) affected the early life phase of this species, and explained up to 85% of the year-to-year variability of the subsequent adult catch. The dynamics of coastal upwelling areas seem to favour paralarva transport to the open ocean during upwelling episodes and concentration at the coast under upwelling relaxation or downwelling conditions (González et al., 2005; Otero et al., 2008). 3.9 Fisheries European vessels fish for O. vulgaris mainly in three areas: the Northeast Atlantic, the Mediterranean, and the eastern central Atlantic off West Africa, although landings into the EU from the latter area (mainly by Spain) have dwindled dramatically as the fishery has increasingly been exploited mainly by Moroccan vessels. The estimated landings for this species were 72 801 t from the eastern central Atlantic in 2008, mostly from western Saharan and Mauritanian waters (and only a small fraction was landed in Europe). This compares with 21 581 t from the Northeast Atlantic and 17 010 t from the Mediterranean (FAO, 2010a). The most recent data available from FAO (Fishstat database) indicate a sharp drop in eastern central Atlantic octopus catches in 2010 (down to ca. 55 000 t), although landings from the Northeast Atlantic and Mediterranean in 2010 were at levels similar to those in 2008. Note that landings data reported to the FAO for the eastern central Atlantic and, to a lesser extent, the Mediterranean have normally been for octopuses in general (i.e. including an unspecified proportion of Eledone spp.). In the Mediterranean, O. vulgaris overtook Sepia officinalis as the most important fished cephalopod species in the late 1970s. However, octopus landings in the Mediterranean have declined fairly consistently since the mid-1980s, and indeed O. vulgaris was overtaken as the most important landed cephalopod by S. officinalis in 2007 (FAO, 2011). The total octopus landings from the Mediterranean in 2010 were 25 300 t, of which 10 300 t were recorded as common octopus and 7000 t as Eledone spp. (FAO, 2011). Estimated total landings of octopods from the ICES area of the Northeast Atlantic in 2010 were ca. 16 600 t, mostly by Portugal and Spain (ICES, 2012), comparable with the 18 300 t recorded for the Northeast Atlantic in the FAO dataset. Although reported total landings have fluctuated from year to year (between 9000 and 18 600 t over the preceding decade), total octopod landings in 2000 and 2010 were similar (ICES, 2012). Octopus vulgaris is taken throughout the year as a target species in bottom trawls and small-scale coastal fisheries using hand-jigs, pots, trammelnets, and traps in depths between 20 and 200 m. Although the majority of landings arise from offshore trawl fisheries, artisanal fisheries have high local economic and social importance in southern Europe (Pereira, 1999). In the Gulf of Cádiz, O. vulgaris is landed by virtually all the artisanal fleets in the region. The main gears used vary from port to port. For example, in Conil, where more than 50% of the artisanal catches of this species are landed, most are taken by a type of hook and line (chivos). Elsewhere in the area, trawls, gillnets, traps, pots, and other types of hooks and lines are used (Silva and Sobrino, 2005). The size range of octopuses captured depends on the size and type of pot used (see Sobrino et al., 2011). In Galicia, ca. 80–90% of landings are by octopus traps (nasas de polbo), with most of the remainder caught using traps targeted at other species. In 2008, 1458 vessels were licensed to use nasas de polbo (Tasende et al., 2009). Otero et al. (2005) used interview data to estimate catches of O. vulgaris by the artisanal fleet in Galicia and showed that true landings are Cephalopod biology and fisheries in Europe: II. Species Accounts | 27 approximately double those reported in official statistics. In the Thracian Sea, octopuses are targeted using pots and taken as bycatch in trammelnets (Lefkaditou et al., 2004). The importance of the species as a resource has led to a requirement for its molecular identification in fishery products (e.g. to detect substitution of Eledone cirrhosa). Espiñeira and Vieites (2012) reported a method to identify fresh, frozen, and processed O. vulgaris using real-time PCR (polymerase chain reaction). Octopus vulgaris is the most abundant and ubiquitous cephalopod species on the Saharan Bank (Northwest Africa from 21 to 26°N). In that area, there are probably two stocks: one off Dakhla (26–23°N) and the other off Cap Blanc (21–19°N) (Murphy et al., 2002). Genetic data indicate the presence of multiple stocks in European waters, with distinct differences between the eastern and western Mediterranean, and Northeast Atlantic and Sahara Bank (Boyle, 2000; Maltagliati et al., 2001; Casu et al., 2002; Cabranes et al., 2008; P. R. Boyle et al. unpublished FAIR-CT96-1520 project data). Although there is no routine assessment of O. vulgaris stocks in European waters, exploited cephalopod stocks in the Saharan Bank fishery (an essential resource for many years for a sector of the Spanish fleet) have been assessed under the auspices of the Fisheries Committee for the Eastern Central Atlantic (e.g. FAO, 1979, 1982, 1987) using production models. The methodology continues to be updated to take advantage of developments in available techniques (e.g. Ono et al., 2012). Cephalopod landings in the European Union are not subject to quota limits. As most octopuses are landed by small-scale fisheries, the activity is mainly regulated at the regional level. Hence, the Galician regional government requires all fishing boats to be licensed. Vessels can use a maximum of five gears, although only one per day, and within specified zones. Fishing is permitted only Monday–Friday, and there are also closed seasons. Minimum landing sizes apply (Tasende et al., 2009). In the case of octopus, a closed season may or may not be imposed. 3.10 Aquaculture Rearing of O. vulgaris is limited to ongrowing subadult individuals captured from the wild, using tanks and cages mainly in Spain, but also in other European Mediterranean countries (Rama-Villar et al., 1997; Iglesias et al., 2000; Aguado and García García, 2002; García García and Aguado Giménez, 2002; Chapela et al., 2006; Rodríguez et al., 2006; Mazón et al., 2007; García García et al., 2009; Domingues et al., 2010; García et al., 2011). On the northwestern Spanish coast, commercial viability is enhanced using readily available mussel-culture rafts as platforms from which to suspend cages. Using fish and crustacean fishery discards as feed, wild subadults can be grown from 800 g to 2.5 kg in 4 months. However, sourcing wild animals for ongrowing from the small-scale fishery would represent an undesirable increase in fishing pressure on the resource and is currently permitted only for pilot schemes. The culture of paralarvae of this species is still under development. At scales other than experimental, the culture of paralarvae is still proving a serious bottleneck to production owing to inadequate artificial diets and high mortality (Navarro and Villanueva 2000, 2003; Villanueva et al., 2004; Iglesias et al., 2004, 2006, 2007; Okumura et al., 2005; Seixas et al., 2010). The lack of a standardized culture method and the absence of appropriate live food to meet paralarval requirements have been identified as two possible causes of this mortality (Iglesias et al., 2007). Iglesias et al. (2004) were able to culture O. vulgaris experimentally through the complete life cycle, using both Artemia and crustacean zoeae as live prey, with 31.5% of 28 | ICES Cooperative Research Report No. 325 paralarvae surviving after 40–45 d, survivors reaching 9.5 ± 1.9 mg dry weight at this point. The octopuses reached a weight of 0.5–0.6 kg at 6 months of age and a final weight of 1.4–1.8 kg at 8 months, the time at which they reached maturity and began to spawn. Moxica et al. (2006) also reared O. vulgaris to the adult stage. Using enriched Artemia as food, they obtained 67% paralarva survival and a dry weight of 1.89 mg after 1 month of culture. In that case, Artemia was cultured with Isochrysis galbana and further enriched with Nannochloropsis sp. Several other authors have also reported successful results from adding Nannochloropsis sp. to the culture tank and as food for Artemia (Hamasaki and Takeuchi, 2000; Hamasaki and Morioka, 2002; Fuentes et al., 2011). Seixas (2009) indicated that Isochrysis galbana mixed with Rhodomonas lens provided the best microalgal combination because of the high level of polyunsaturated fatty acids (PUFAs) (in Isochrysis galbana) and very high level of proteins (in Rhodomonas lens). These studies have together shown that a mixed live diet of enriched Artemia and crustacean zoeae is the most balanced diet for producing the best growth and survival results in the paralarva phase, achieving dry weights threefold higher than obtained from feeding with Artemia enriched with microalgae. Nevertheless, this approach is currently not transferable to a commercial scale owing to the limited availability of live zoeae. 3.11 Future research, needs, and outlook Important topics for future research include investigations on early life stages and the influence of environmental conditions on wild octopus populations. Further, the development of inert diets to feed the paralarvae or microencapsulated products to produce enriched Artemia with a similar nutritional composition to crustacean zoeae is important for solving the paralarva rearing problem. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Eledone cirrhosa Horned octopus | 29 30 | 4 ICES Cooperative Research Report No. 325 Eledone cirrhosa (Lamarck, 1798) Paola Belcari, Paolo Sartor, Patrizia Jereb, Evgenia Lefkaditou, Graham J. Pierce, Uwe Piatkowski, Teresa Borges, and A. Louise Allcock Common names Élédone commune, poulpe, poulpe blanc, pieuvre blanche (France); Μοσκιός [moschios] (Greece); moscardino bianco (Italy); polvo do alto, polvocabeçudo (Portugal); pulpo blanco (Spain); horned octopus, lesser octopus, curled octopus (UK) (Figure 4.1). Synonyms Octopus cirrhosus Lamarck, 1798, Sepia cirrhosa: Bosc (1802), Eledone aldrovandi Figure 4.1. Eledone cirrhosa. Dorsolateral view. Montfort, 1802, Octopus leucoderma San From Guerra (1992). Giovanni, 1829, Eledone genei Verany, 1839, Eledone ambrosiana Risso, 1854, Eledone halliana Rochebrune, 1884, Pallia sepioidea Rochebrune, 1884, Moschites cirrosa: Pfeffer (1908), Ozaena cirrhosa: Adam (1934), Moschites cirrhosa zetlandica Russell, 1922. 4.1 Geographic distribution The horned octopus, Eledone cirrhosa (Lamarck, 1798), is found in the Northeast Atlantic from ca. 66–67°N south to Moroccan waters and throughout the Mediterranean Sea (Norman et al., 2014) (Figure 4.2). In the northernmost part of its distribution, the species extends to southern Iceland, the Faroe Islands (Bruun, 1945), and the west coast of Norway (Nordgård, 1923; Grieg, 1933), where it seems to reach Ostnesfjord in Lofoten, although it is rarely found north of Trondjemsfjord (Grieg, 1933). Old records in the Skagerrak and Kattegat have been reviewed by Hornbörg (2005). It is a common species in Irish and British waters, abundant along the entire Scottish coast, and common in the Celtic Sea and English Channel (Massy, 1928; Stephen, 1944; Rees, 1956; Boyle, 1983b; Lordan et al., 2001a). It is present in the North Sea (Grimpe, 1925; De Heij and Baayen, 2005; Oesterwind et al., 2010), though more abundant in the northeastern and central eastern areas (De Heij and Baayen, 2005), and extends south along the Atlantic coasts of France, Spain, and Portugal, although the southern limits of its distribution are uncertain (ca. 33°N; Guerra, 1992). Eledone cirrhosa is widespread throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), including western and central Mediterranean waters (Mangold-Wirz, 1963a; Sánchez, 1986a; Würtz et al. 1992a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005, 2011; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia, 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 2002; Lefkaditou et al., 2003b; Duysak et al., 2008; Mienis et al., 2011). The species has been recorded in the Sea of Marmara (Ünsal et al., 1999). Cephalopod biology and fisheries in Europe: II. Species Accounts | 31 Figure 4.2. Eledone cirrhosa. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 4.2 Taxonomy 4.2.1 Systematics Coleoidea – Octopodiformes – Octopoda – Octopodidae – Eledone. 4.2.2 Type locality Not indicated. 4.2.3 Type repository Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. Holotype. Specimen not found [fide Lu et al. (1995)]. 4.3 Diagnosis 4.3.1 Paralarvae Findings of paralarvae in the Mediterranean and in the Atlantic were reported by Mangold-Wirz (1963a). More recently, paralarvae of E. cirrhosa have been collected around the British Isles (Collins et al., 2002) and in the Aegean Sea (Salman et al., 2003). 32 | ICES Cooperative Research Report No. 325 4.3.2 Juveniles and adults Eledone cirrhosa is a mediumsized species with a maximum body weight <1 kg in the Mediterranean and up to 2 kg in the northern parts of its distribution. Most studies that report body weight do not report mantle length, although Belcari and Sartor (1999a) refer to animals reaching 175 mm ML. The mantle is short and ovoid. Figure 4.3. Eledone cirrhosa. Dorsal (left) and ventral (right) The head is narrower than views. Photos: Domenico Capua. the mantle. Live animals range from orange to yellow, through orange–red to reddish–brown on the dorsal surface, and have greenish iridescence on the ventrum (Figure 4.3). The dorsal surface is covered with numerous warts. A whitish line encircles the lateral periphery of the mantle. There is a cirrhus near each eye. The arms are moderately short, and the suckers are uniserial. The third right arm of males is hectocotylized and is shorter (69–76%) than its opposite left arm. The ligula is very short (3–4% of the length of the hectocotylus), and there is no calamus. The tips of the other arms are modified in males through transverse compression of the suckers (Naef, 1921/1923; Nesis, 1982/1987; Roper et al., 1984; Mangold and Boletzky, 1987; Guerra, 1992). The upper and lower mandibles (beaks) are illustrated in Figure 4.4; see Clarke (1986) for further description. Figure 4.4. Eledone cirrhosa. Lower beak (left) and upper beak (right). Note that in life, the orientation of the lower beak relative to the upper beak would be rotated vertically by 180° (see diagram for Octopus vulgaris in Nixon, 1969). Photo: Evgenia Lefkaditou. 4.4 Life history Eledone cirrhosa probably typically lives for 2 years. Breeding is seasonal, with the peak of spawning varying according to region. The paralarva has a short planktonic phase. Cephalopod biology and fisheries in Europe: II. Species Accounts 4.4.1 | 33 Egg and juvenile development Fertilization is completely internal; the male spermatangia reach the ovary before the sperm are released. There are few reports of direct observations on eggs in natural environments. Mangold et al. (1971) commented that there was only one record of an egg mass found in the sea, near the Shetland Islands, as detailed in Stephen (1944). Fertilized eggs and development to hatching have been observed in aquaria, with almost mature ovarFigure 4.5. Eledone cirrhosa. Mature eggs ian eggs reaching 7.2 mm in length (Manfrom oviducts of a spawning female. Photo: gold-Wirz, 1963a) (Figure 4.5). Hatching ocPaolo Sartor. curs after 3–4 months, usually during April– July, in temperatures of 14–18°C. The newly hatched paralarvae (4.5 mm ML) are truly planktonic (Mangold et al., 1971), but that stage is thought to have a short duration (Collins et al., 2002). Relini and Orsi Relini (1984) collected individuals of 15 mm ML in the Ligurian Sea from the end of January, and Lloret and Lleonart (2002) reported finding the smallest E. cirrhosa (30 mm ML) in landings from the northwestern part of the Mediterranean in March. 4.4.2 Growth and lifespan Eledone cirrhosa is a medium-sized octopus. Most specimens caught are <160 mm mantle length (ML), although, occasionally, individuals of larger size, up to 175 mm ML, are captured, both in the Mediterranean (Belcari and Sartor, 1999a; Cuccu et al., 2003b) and in the Atlantic off Portugal (A. Moreno, pers. comm.). Females attain larger size than males, which generally do not exceed 110–120 mm ML, but occasionally can reach 135 mm ML. On Galician coasts, females can reach 191 mm ML (1150 g) and males 158 mm ML (634 g) (Regueira et al., 2013). In the North Sea off Aberdeen, females may reach 2000 g and males 750 g (Boyle, 1997). Numerous studies on growth have reported length–weight relationships (Table 4.1). Comprehensive growth studies, defining von Bertalanffy growth parameters, are available for populations in various Italian waters (Agnesi et al., 1998; Cuccu et al., 2003b; Orsi Relini et al., 2006; Giordano et al., 2010). In a recent study on the biology and fishery of E. cirrhosa in the Ligurian Sea, Orsi Relini et al. (2006) suggested a linear growth model for recruits indicating a maximum age of 300 d, with the function ML (mm) = 0.166 × time (d) + 5.946. During sexual maturation, growth of males does not cease completely, as it does in females (Orsi Relini et al., 2006). Table 4.1. Eledone cirrhosa. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Northern Galicia 0.862 2.38 M Regueira et al. (2013) 0.556 2.60 F 0.490 2.61 M 0.404 2.76 F 0.848 2.30 M 0.377 2.73 F Western Galicia Western Portugal 34 | ICES Cooperative Research Report No. 325 Western Mediterranean 1.62 2.27 All Sea Gulf of Lions Ligurian Sea Adriatic Sea P. Sánchez, pers. comm. 0.86 2.61 F 0.91 2.57 M 0.679 2.47 F 0.768 2.38 M 0.726 2.43 All 0.159–0.212 2.85–2.9 F 0.233–0.247 2.79–2.89 M 0.394 2.713 All Moriyasu (1983) Massi (1993) De Rossi (2000) G. Marano, pers. comm. 0.336 2.281 All G. Marano, pers. comm. Northern Tyrrhenian Sea Central Tyrrhenian Sea Southern Tyrrhenian 0.26–0.47 2.60–2.88 F 0.32–0.54 2.52–2.79 M 0.56 2.56 F 1.76 1.96 M 1.46 2.46 F 0.56 2.15 M 0.841 2.51 F 0.915 2.43 M Belcari et al. (1990a) Agnesi et al. (1998) Giordano et al. (2010) Sea Thracian Sea Lefkaditou et al. (2007) Forsythe and van Heukelem (1987) reported instantaneous relative growth rates of between 2.8% BW d–1 in the smallest individuals and 0.7% BW d–1 in the largest. Boyle and Knobloch (1982a) observed that, at 10°C, the species can grow from 10 g to 1 kg in 270 d. In captivity, they recorded growth rates of up to 3.5% BW d–1 in individuals of 100 g BW, falling to ca. 1.5% BW d–1 at body mass >500 g. Although E. cirrhosa is short-lived and semelparous (Mangold-Wirz, 1963a; Guerra, 1992), it exhibits considerable plasticity in its life cycle throughout its geographic range (Hastie et al., 2009a). In fact, its lifespan has been interpreted in various ways. A combination of a 1- and 2-year cycle was proposed for the North Sea, depending, respectively, on fast-growing, early-maturing animals and slower-growing individuals (Boyle and Knobloch, 1982a; Boyle, 1983b; Boyle et al., 1988). In the Mediterranean, growth studies on young individuals show that sexual maturity can be achieved only in the second year of life (Mangold-Wirz, 1963a). The strictly seasonal reproduction gives one cohort year–1 and, after 1 year of growth, juveniles have not reached reproductive size. Given that death follows reproduction, the lifespan of the majority of individuals can be estimated to be ca. 2 years, an interpretation common for E. cirrhosa from the Mediterranean (e.g. Moriyasu, 1981; Belcari and Sartor, 1999a; Sánchez et al., 2004; Giordano et al., 2010). However, 2- and 3-year cycles have been proposed for the species based on individual growth and maturation studies and length-frequency analyses of different local stocks. Recent papers, with analyses of length-frequency distributions covering different seasons and/or the complete spatial distribution of E. cirrhosa (Lefkaditou and Papacostantinou, 1995; Cuccu et al., 2003b; Orsi Relini et al., 2006), show both the presence of a fraction of adult non-reproducing individuals during the reproductive season and polymodal sizes in spawners. Consequently, a total lifespan of 3 years has been assumed, even though the vast majority of the adult population lives for a maximum of 2 years. The fraction of the population reproducing at age 3 has Cephalopod biology and fisheries in Europe: II. Species Accounts | 35 been estimated at <10% of adult individuals, but is considered of great biological value in terms of reproductive potential and genetic diversity (Orsi Relini et al., 2006). Recent developments in methods for visualizing potential growth rings in stylets mean that direct age determination of individuals may be possible in future (Barratt and Allcock, 2010). 4.4.3 Maturation and reproduction In samples collected by Boyle and Knobloch (1982b) in Scottish waters, females were always more numerous than males, the ratio of females to males being 7:1 overall during September 1976 – December 1979. This could be at least partly related to difference in catchability attributable to different body sizes: in 1978, the average female size was 594 g compared with 290 g for males. Regueira et al. (2013) also found that the overall sex ratio (ca. 3:1) in their sample from the northwestern Iberian Peninsula was biased towards females. For the Mediterranean, Boyle (1997) noted that the sex ratio was 1:1 in deeper water, but biased towards females in shallow water in spring, which he interpreted as a shoreward migration for breeding. Males are more precocious than females, attain maturity at a smaller size, and their period of maturation is longer. Fully mature females are rarely found. In the Atlantic off Portugal, 50% of females are mature at 105 mm ML, whereas 50% of males are mature at 80 mm ML (A. Moreno, pers. comm.). Along the Iberian Atlantic coast, animals mature larger at higher latitudes. Size at 50% maturity (MLm50%) for males was 108.9 mm on the north coast of Galicia, 99.25 mm on the west coast of Galicia (i.e. farther south), and 91.4 mm on the west coast of Portugal. The corresponding values for females were 134.5, 121.4, and 100.8 mm, respectively (Regueira et al., 2013). In the Mediterranean, 50% of females are mature at a length of 80–120 mm ML, and 50% of males are mature at 55–90 mm ML (Palumbo and Würtz, 1983–1984; Relini et al., 1994; Tursi et al., 1995; Agnesi et al., 1998; Cuccu et al., 2003b). However, Boyle and Knobloch (1982b) noted that female E. cirrhosa become mature at a wide range of body sizes and concluded that maturity was not predictable from body size. Boyle and Thorpe (1984) showed that gonad maturation is linked to an increase in the size of the optic gland. However, as they also noted, the lack of synchrony in individual maturation is an obstacle to the idea that environmental cues might trigger the activity of the optic glands. Eledone cirrhosa displays seasonal sexual maturity (Belcari et al., 1990b). Across the Mediterranean, regional differences in the timing of spawning have been reported. Generally, sexual maturity occurs earlier in the western basin (spring–summer) than in the eastern basin (summer–autumn) (Belcari and Sartor, 1999a; Lefkaditou et al., 2000; Belcari et al., 2002a; Cuccu et al., 2003b; Orsi Relini et al., 2006; Giordano et al., 2010). In the North Sea, females mature mainly during July–September, and spawning takes place immediately thereafter (Boyle, 1983a; Boyle and Knobloch, 1983), although those authors stress that maturation can occur at any time of year. Indeed, a contemporaneous study on male maturity (Boyle and Knobloch, 1984) found no evidence of seasonality in maturity. In northwestern Iberian waters, the main spawning season is in May and June (Regueira et al., 2013). In Portuguese waters, mature males are found during February–July and mature females during May–August (A. Moreno, pers. comm.). According to Boyle and Chevis (1992), a significant proportion of eggs fails to develop beyond 2–3 mm long (the size at which vitellogenesis occurs), and those eggs subsequently degenerate. Fecundity estimations vary greatly according to area and maturation stage of ovary and eggs. The mean number of eggs at all stages of maturity was ca. 9000 when estimated for females from the North Sea and 5500 for females from the 36 | ICES Cooperative Research Report No. 325 Catalan Sea (Boyle et al., 1988). Regueira et al. (2013) estimated potential fecundity in the northwestern Iberian Peninsula as 2452.88  36.4 oocytes per ovary, based on a sample of almost 700 females; potential fecundity was positively correlated with both mantle length and body weight. In a study from the northern Tyrrhenian Sea, an average of 2000 eggs in mature ovaries was reported (Rossetti, 1998). According to Regueira et al. (2013), mature males have an average of 86.55  1.19 spermatophores, with an average length of 44.97  0.29 mm. 4.4.4 Natural mortality The main mortality event in the life of E. cirrhosa appears to follow reproduction. Records of post-spawning or spent specimens are very rare. Few spent females have been recovered, indicating post-reproductive mortality (Mangold-Wirz, 1963a; Guerra, 1992; Tursi et al., 1995). However, modal progression analysis suggests that a small fraction of adults (5–10%) survive until the following reproductive season in Italian waters (Cuccu et al., 2003b; Orsi Relini et al., 2006). 4.5 Biological distribution 4.5.1 Habitat Eledone cirrhosa is a typical soft-bottom, eurybathic species. It lives over a wide bathymetric range, generally down to 700 m. It has been reported from 770 m near the Faroe Islands (Massy, 1928), although most catches are made over a smaller depth range, generally from 50 to 300 m (Boyle, 1997; Belcari and Sartor, 1999a; Belcari et al., 2002a; Orsi Relini et al., 2006). Generally, females dominate in water 30–80 m deep, an even sex ratio is reported in the range 100–200 m, and males dominate in deeper water (Mangold-Wirz, 1963a; Palumbo and Würtz, 1983–1984; Tursi et al., 1995; Boyle, 1997; Orsi Relini et al., 2006). 4.5.2 Migrations Although generally thought of as rather sedentary (Roper et al., 1984), evidence for a pattern of seasonal migration in the Mediterranean is available from analyses of sex ratio and maturity states from a range of depths. The deep-water population (100–200 m) normally has equal numbers of males and females, but trawls in shallower water (60–90 m) in spring catch an increased number of maturing females. This seasonal sex segregation is interpreted as a shoreward (shallower) migration of females for breeding (Boyle, 1997). However, downward vertical migrations linked to spawning have also been proposed. In Italian waters, there are more males than females at depths >300 m (Belcari and Sartor, 1999a). In the Ligurian Sea, Orsi Relini et al. (2006), analysing 10 years of biological information, found a similar pattern and suggested that bathyal hard substrata provide suitable seabed for egg laying and attachment. 4.6 Trophic ecology 4.6.1 Prey Eledone cirrhosa is a carnivorous species and an active predator. Its diet consists mainly of decapod crustaceans (Table 4.2), mostly alpheids and brachyurids, as observed in Scottish waters (Boyle, 1983b, 1986) and different areas of the western Mediterranean Sea (Moriyasu, 1981; Sánchez, 1981; Auteri et al., 1988). Fish, cephalopods, gastropods, and ophiuroids have also been encountered in its gut contents, and cannibalism has been observed (Guerra, 1992). Cephalopod biology and fisheries in Europe: II. Species Accounts | 37 Table 4.2. Prey composition of Eledone cirrhosa, as known from studies in the western Mediterranean Sea and Scottish waters (compiled from Moriyasu, 1981 1; Sánchez, 19812; Boyle, 1983b3, 19864; Boyle et al., 19865; Auteri et al., 19885). Taxon Species Osteichthyes Gobiidae Deltentosteus quadrimaculatus (four-spotted goby)2 Merlucciidae Merluccius merluccius (European hake)1 Soleidae Solea solea (common sole)1 Crustacea Decapoda Macrura rep- indet.2,6 Homarus spp.(lobster)3, Nephrops norvegicus (Norway lobster)3,4,5 tantiaAstacidea Pleocyemata- Galathea intermedia1, Paguridae indet.1,6, Pisidia longirostris1 Anomura Pleocyemata- Cancer spp.3, Goneplax rhomboides1, Goneplax spp.2, Leucosiidae in- Brachyura det.1,6, Liocarcinus spp.5, Majidae indet.6, Monodaeus couchii2, Portunidae indet.6, indet.2 Pleocyemata- Alpheus glaber1,2, Alpheus spp.6, Crangonidae indet.5,6 Caridea Pleocyemata- Jaxea nocturna1 Gebiidea Cephalopoda indet.2,6 Myopsida Alloteuthis media1 Octopoda Eledone cirrhosa1 Sepioidea Sepiolidae spp.1,4 Gastropoda indet.1 Bivalvia indet.4 Echinodermata Ophiuroidea Polychaeta 4.6.2 Ophiothrix quinquemaculata1, indet.4,6 Aphroditidae indet.2, indet.1,6 Predators Whales, seals, and fish are considered to be the most important predators of E. cirrhosa (e.g. Santos et al., 1999; Brown et al., 2001; Velasco et al., 2001). Eledone cirrhosa is an important component of the summer diet of harbour seals (Phoca vitulina) in the Moray Firth in some years (Tollit and Thompson, 1996) as well as a prominent component of the diet of some cetaceans (Table 4.3). Table 4.3. Known predators of Eledone cirrhosa in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopoda Giant squid (Architeuthis dux) Lordan et al. (1998a) Veined squid (Loligo forbesii) Guerra and Rocha (1994) Blue shark (Prionace glauca) Clarke and Stevens (1974) Cuckoo ray (Raja naevus) Ellis et al. (1996) Chondrichthyes 38 | ICES Cooperative Research Report No. 325 Lesser spotted dogfish (Scylio- Ellis et al. (1996) rhinus canicula) Greater spotted dogfish Ellis et al. (1996) (Scyliorhinus stellaris) Spotted ray (Raja montagui) Ellis et al. (1996) Spurdog (Squalus acanthias) Ellis et al. (1996) Thornback ray (Raja clavata) Ellis et al. (1996), Farias et al. (2006) Tope shark (Galeorhinus Ellis et al. (1996) galeus) Osteichthyes Albacore (Thunnus alalunga) Salman and Karakulak (2009), Romeo et al. (2012) Atlantic cod (Gadus morhua) Du Buit (1989), Daly et al. (2001) Haddock (Melanogrammus Daly et al. (2001) aeglefinus) Ling (Molva molva) Daly et al. (2001) Monkfish (Lophius piscatorius) Daly et al. (2001), Velasco et al. (2001), Laurenson and Priede (2005) Pinnipedia Swordfish (Xiphias gladius) Romeo et al. (2009, 2012) Grey seal (Halichoerus grypus) Pierce et al. (1991a), Strong (1996) Harbour seal (Phoca vitulina) Pierce et al. (1991b), Tollit and Thompson (1996), Brown et al. (2001), Pierce and Santos (2003), Kavanagh et al. (2010) Pinnipedia Monk seal (Monachus mona- Pierce et al. (2011) chus) Cetacea Bottlenose dolphin (Tursiops González et al. (1994a), Santos et al. truncatus) (1997, 2001a, 2005a, 2007) Common dolphin (Delphinus González et al. (1994a), Silva (1999a), delphis) Santos et al. (2004a), De Pierrepont et al. (2005) Harbour porpoise (Phocoena Santos et al. (2004b, 2005b) phocoena) Long-finned pilot whale (Glo- González et al. (1994a) bicephala melas) Northern bottlenose whale M. B. Santos, pers. comm. (Hyperoodon ampullatus) Risso’s dolphin (Grampus griseus) Clarke and Pascoe (1985), González et al. (1994a), Blanco et al. (2006), Bearzi et al. (2011), MacLeod et al. (2014) Sperm whale (Physeter mac- Santos et al. (1999) rocephalus) White-beaked dolphin (La- Canning et al. (2008) genorhynchus albirostris) 4.7 Other ecological aspects 4.7.1 Parasites Hochberg (1983, pers. comm.) recorded fungi (Ulkenia amoeboidea, Cladosporium sphaerospermum), ciliates (Chromidina coronata), dicyemids (Dicyemennea eledones, Dicyemennea Cephalopod biology and fisheries in Europe: II. Species Accounts | 39 lameerei), helminths including digeneans and cestodes (Phyllobothrium sp., Scolex p. unilocularis, Nybelinia lingualis, Eutetrarhynchus sp.), nematodes (unidentified larvae), and copepods (Pennella “varians”) in E. cirrhosa. Ciliates and dicyemids were found in the kidneys and cestodes in the crop. Polglase (1980) attributed a pathological condition in E. cirrhosa to the presence of thraustochytrid and labyrinthulid fungi. These fungi may be found in skin lesions and can present a major problem for maintaining E. cirrhosa in aquarium tanks (Hochberg, 1983). The nematode Anisakis simplex has been reported from E. cirrhosa in Galician waters (Abollo et al., 1998). Ascaridoids of the genus Hysterothylacium have been reported from the digestive tract, and copepods of the genus Pennella from the gills of E. cirrhosa caught in the northern Tyrrhenian Sea (Gestal et al., 1999). Polglase (1980) refers to the presence of thraustochytrids and labyrinthulids, parasitic protists more usually found in marine algae and seagrasses, in E. cirrhosa. 4.7.2 Contaminants The digestive gland, branchial hearts, and kidney are the main sites of concentration for heavy metals: the digestive gland accumulates most silver, cadmium, cobalt, copper, iron, lead, and zinc; branchial hearts have high concentrations of copper, nickel, and vanadium; and the kidney has high concentrations of manganese, nickel, and lead (Miramand and Bentley, 1992). The species is a strong accumulator of mercury, whose concentration in the muscle tissue was correlated with length in both sexes, but with a reduction in mercury uptake in females near spawning (Rossi et al., 1993). Cadmium concentrations in the mantle decrease over the course of the life cycle, possibly related to a detoxification mechanism involving selenium (Barghigiani et al., 1993). 4.7.3 Environmental effects Eledone cirrhosa abundance and distribution vary greatly among the various fishing areas of the Mediterranean and North Atlantic and are related to depth and shape of the continental shelf (Lefkaditou et al., 2000; González and Sánchez, 2002). Fluctuations in numbers and biomass indices of E. cirrhosa have been linked to climatic factors (e.g. the North Atlantic Oscillation) by a number of authors (e.g. Lloret et al., 2001; Sánchez et al., 2004; Orsi Relini et al., 2006). Sobrino et al. (2002) showed that E. cirrhosa abundance in the Gulf of Cádiz was highly negatively correlated with rainfall in the previous year, and also negatively correlated with river discharges and sea surface temperature. Sea surface temperature values >20°C in June (before the start of the fishing season) were associated with reduced catches. 4.7.4 Behaviour “Sand covering”, similar to the behaviour seen in Sepia spp. and various species of sepiolid, was described for the first time in the lesser octopus by Guerra et al. (2006). The animals displayed a burrowing/burying behaviour lasting ca. 50 s. The behaviour continued until the animal was totally covered except for its eyes. Under aquarium conditions, E. cirrhosa is relatively sedentary, spending most of its time in the shelter of dens or rocks or at the edges of the tank space. Time-lapse photography shows that long quiescent periods are interspersed with periods of activity when the animal moves throughout the tank space and often swims. These active spells presumably represent periods of hunting or foraging behaviour (Boyle, 1997). 4.8 Fisheries The horned octopus is a commercially important species and has great commercial 40 | ICES Cooperative Research Report No. 325 value in most areas, especially in the western Mediterranean (Mangold and Boletzky, 1987; Sartor et al., 1998a; Relini et al., 1998), although it is routinely discarded by Scottish boats (Pierce et al., 2010) and is among the cephalopod species most commonly discarded by Spanish boats fishing in northern waters (Santos et al., 2012). In FAO FISHSTAT data for the Northeast Atlantic, E. cirrhosa has been recorded separately only since 2000, and the maximum catch recorded (365 t in 2004) is likely to represent only a small fraction of the true landings, most of which are probably subsumed within the “octopuses, etc. nei” (octopus not elsewhere included) category (13 825 t landed in 2004). Landings of octopus reported to ICES are not disaggregated by species. In the Mediterranean, according to FAO data, landings of Eledone spp. (combined for E. cirrhosa and E. moschata) and Octopus vulgaris have been recorded separately since 1962. However, the quantity of landings assigned to the category “octopuses, etc. nei” was up to fivefold that assigned to Eledone spp. until 2004, after which reported landings in the two categories have been similar, with landings of Eledone spp. peaking at almost 9600 t in 2005. Catches of E. cirrhosa are almost entirely taken by bottom trawl. In the Northeast Atlantic, E. cirrhosa is present in the landings of Portugal (Fonseca et al., 2008), Spain, and (rarely, given that it is usually discarded) Scotland, but there appears to be little commercial interest in the species (Pierce et al., 2010). In Scottish waters, it can constitute a substantial proportion of the bycatch for trawlers operating close to shore, especially those fishing on soft bottoms for Norway lobster (Nephrops norvegicus), although such bycatches are discarded. Eledone cirrhosa is the only Eledone species present in northern Spanish waters, where it is landed by the bottom-trawl fishery as bycatch, although its commercial value in that region is very low. Although there are some minor differences by port, almost all E. cirrhosa individuals captured in the Mediterranean are landed; the discard percentage is usually <10% (Sartor et al., 1998a). Because of the biological characteristics of the species, there is seasonal variability in the landings, as reported in studies of the landings of Spanish, Italian, and Greek fleets (Sánchez and Martin, 1993; Belcari and Sartor, 1993; Belcari et al., 1998; Tsangridis et al., 2000; Lloret and Lleonart, 2002). Recruitment of E. cirrhosa to the trawl fishery is from January on, mostly in spring and summer, at an estimated age of 5–7 months. Recruits are mainly distributed on the continental shelf, especially where the shelf is wide (Belcari and Sartor, 1999a; Belcari et al., 2002a; Lloret and Lleonart, 2002; Orsi Relini et al., 2006). The highest densities in the Mediterranean have been found in the Gulf of Lions, the Ligurian and northern Tyrrhenian seas, and in the northern Aegean Sea (Belcari et al., 2002a). In the Mediterranean, E. cirrhosa is marketed in two different size categories (Belcari et al., 1998; Belcari and Sartor, 1999a; Orsi Relini et al., 2006; Giordano et al., 2010). Small specimens, generally <50 mm ML, have great economic value and, in some regions, are abundant in the market, being the target of the multispecies trawl fishery in spring and summer that coincides with the recruitment period of the species (Relini and Orsi Relini, 1984; Belcari et al., 1998; Sánchez et al., 2004; Orsi Relini et al., 2006). The fishery for these juvenile E. cirrhosa (0 age group, known locally as “popets” in Catalonia and “moscardini” in Tuscany) is an important activity, particularly in three western Mediterranean areas: the Catalan coast, the Ligurian Sea, and the northern Tyrrhenian Sea, where the species is more abundant (Belcari et al., 2002a). Even though there is no minimum legal size applied to E. cirrhosa catches, this form of trawling is restricted by the present EC regulations on mesh size. Cephalopod biology and fisheries in Europe: II. Species Accounts | 41 Tentative stock assessments have been performed for the species in different areas of the western Mediterranean. Local stocks may be underexploited, at equilibrium, or slightly overexploited, depending on the area (Agnesi et al., 1998; Orsi Relini et al., 2006; Giordano et al., 2010). Natural mortality rates estimated on various local stocks with different methods vary from 0.58 to 1.45 (Agnesi et al., 1998; Orsi Relini et al., 2006; Giordano et al., 2010). 4.9 Future research, needs, and outlook Important topics for future research on the species include investigations on spawning sites, fecundity, description of early life stages, increment reading of beaks and stylets, and genetic studies for stock identification. Further studies on appropriate stock assessment methods are also desirable. Previous taxonomic work (F. G. Hochberg, pers. comm.) suggests that E. cirrhosa actually comprises two species: one within the Mediterranean and one in the Northeast Atlantic. This issue could be resolved by raising the subspecies E. cirrhosa zetlandica Russell, 1922, which was described from around Scotland, to specific status (F. G. Hochberg, pers. comm.). Further study of parasites in European cephalopods could also help to clarify taxonomy. 42 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Eledone moschata Musky octopus Cephalopod biology and fisheries in Europe: II. Species Accounts 5 | 43 Eledone moschata (Lamarck, 1798) Ignacio Sobrino, Ana Moreno, Patrizia Jereb, Eduardo Balguerias, Sonia Seixas, Graham J. Pierce, Evgenia Lefkaditou, and A. Louise Allcock Common names Elédone musquée (France); Μοσκιός [moschios] (Greece); moscardino rosso, moscardino muschiato (Italy); polvo cabeçudo, polvomosqueado, polvo-de-cheiro (Portugal); pulpo cabezón, pulpo almizclado (Spain); musky octopus (UK) (Figure 5.1). Synonyms Octopus moschatus Lamarck, 1798, Eledona moschata: Risso (1854). 5.1 Figure 5.1. Eledone moschata. Dorsolateral view. From Guerra (1992). Geographic distribution The musky octopus, Eledone moschata (Lamarck, 1798), lives in the Northeast Atlantic and in the Mediterranean Sea (Norman et al., 2014; Figure 5.2). In the Northeast Atlantic, it is occasionally found off Portugal as far north as ca. 40°N (Lourenço et al., 2008) and is abundant in Portuguese and Spanish waters of the Gulf of Cádiz (Guerra, 1982, 1992; Reis et al., 1984). It is widespread throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), including western and central Mediterranean waters (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), and, though occasionally less abundant, the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak et al., 2008). The species has been recorded in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Primarily a Mediterranean species, the southern limits of the Northeast Atlantic distribution of E. moschata remain uncertain. 44 | ICES Cooperative Research Report No. 325 Figure 5.2. Eledone moschata. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 5.2 Taxonomy 5.2.1 Systematics Coleoidea – Octopodiformes – Octopoda – Octopodidae – Eledone. 5.2.2 Type locality Not stated in original description. 5.2.3 Type repository Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. The type does not appear to be extant (see Lu et al., 1995). 5.3 Diagnosis 5.3.1 Eggs and hatchlings Eggs are joined by their short stalks in clusters and attached to a substratum. The clusters contain 3–10 eggs, and they have no central stem. The eggs are elongate, measure 12–16 mm long and 4–5 mm wide (Mangold, 1983b). In the Gulf of Cádiz, mature eggs are generally smaller, on average 10.9 mm long (Silva et al., 2004). Hatchlings measure 25–30 mm TL and 10–12 mm ML, ca. 10% of the adult size. At hatching, each arm already bears 30 suckers and is longer than the body (Mangold, 1983b). 5.3.2 Juveniles and adults The skin is smooth to very finely granulose; there is no ridge around the lateral periphery of the mantle. The arms are subequal in length with uniserial suckers. The web is moderately deep, ca. 30% of arm length. In mature males, the third right arm is hectocotylized (Figure 5.3) and is 85–90% of the length of the third left arm. The ligula is Cephalopod biology and fisheries in Europe: II. Species Accounts | 45 short (ca. 3% of arm length), and there is no calamus. The distal tips of all other arms of males are modified with two parallel series of flattened laminae or platelets. Internally, the gills have 11–12 filaments per demibranch. Live animals exude a very prominent, musk-like odour, reportedly from glands in the skin. Live animals are greyishbrown with blackish-brown blotches on the dorsum (Mangold and Boletzky, 1987; Relini et al., 1999; Norman et al., 2014). The beaks are illustrated in Figure 5.4. Figure 5.3. Eledone moschata. Right arm III hectocotylized. Photo: Carlos Farias. Figure 5.4. Eledone moschata. Lower beak (left) and upper beak (right). Photos: Evgenia Lefkaditou. 5.4 Remarks Norman et al. (2014) list no synonyms. Norman and Hochberg (2005) listed Eledonenta microsicya Rochebrune, 1884 as a synonym of Eledone moschata. Robson (1932) suggested that "Eledonenta microsicya" should be placed in Eledone and that it was more similar to E. moschata than to other species of Eledone. Nonetheless, he did not synonymize the two species. Silas (1968) treats the species as Eledonenta microsicya, but noting Robson's (1932) opinion. The original description (Rochebrune, 1884) is strongly suggestive of Eledone (e.g. "cupules... sur un seul rang"), but his description of a dirty yellow animal with small black dots and large bluish spots "jaune sale, finement piquete de tres petits points noirs et orne de larges taches bleuatres" does not match E. moschata. Therefore, the identity of E. microsicya remains unsolved, but we do not believe it to be synonymous with E. moschata. 5.5 Life history In contrast to E. cirrhosa, hatchlings of E. moschata immediately adopt a benthic mode of life. The breeding cycle is seasonal, with one or two peaks in activity, the main one often during the first quarter of the year. There may be alternating long and short life cycles. 46 | ICES Cooperative Research Report No. 325 5.5.1 Egg and juvenile development Few records have been published on naturally occurring eggs. Egg masses have been collected in shallow waters in the northern Adriatic Sea. In captivity, embryonic development lasts 4–6 months, depending on temperature (Mangold, 1983b). After hatching, animals adopt the adult benthic mode of life and immediately begin to feed on live crabs of their own size. A preference for a crustacean diet is clear from the very early stages on (Boletzky, 1975a). Mean growth rate of hatchlings is ca. 6.2% of body weight d–1 up to 10 g, 3% d–1 between 10 and 100g, and 0.8% d–1 thereafter (Mangold, 1983b). 5.5.2 Growth and lifespan Eledone moschata reaches a maximum size of 150 mm ML and 640 g body weight in the Atlantic (Silva et al., 2004) and 188 mm ML and 1414 g body weight in the Mediterranean Sea (Akyol and Şen, 2007). Boletzky (1975a) reared it, recording a growth rate of 6.6% BW d–1 for the first month after hatching and 3.6% BW d –1 for the subsequent 3 months. Hatchlings weighed 0.3 g, reaching 2.2 g BW after 1 month and 55 g at 4 months. Forsythe and van Heukelem (1987) give values for instantaneous relative growth rates ranging from 6.94% BW d –1 in the smallest animals to 0.99% BW d–1 in animals of 50 g BW. Length–weight relationships show some regional variation (Table 5.1). The proposed life cycle model of this species in the northwestern Mediterranean is based on the alternation of short-lived and long-lived life cycles (Mangold, 1983b; Silva et al., 2004). This model seems to apply in the Gulf of Cádiz. Recruitment is in September and October and presumably originates from the long-living fraction of mature females that spawned at the beginning of the spawning season. Another recruitment pulse is detected in January and February, which is related to the short-lived fraction of the population that spawned at the end of the spawning season. Favourable environmental conditions may lead to faster growth and more rapid sexual development of the short-lived fraction of the population. The smaller spawning peak observed in October in the Gulf of Cádiz could be a consequence of this phenomenon (Mangold, 1983b; Ezzeddine-Najai, 1997; Silva et al., 2004). Lifespan is probably up to 2 years (e.g. Mangold, 1983b). Table 5.1. Eledone moschata. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Portugal 1.0048 2.4 F Lourenço et al. (2008) 0.6325 2.5 M 0.8652 2.46 All 0.3573 2.660 F 0.2613 2.794 M 0.3233 2.702 All 0.3323 2.814 F Gulf of Cádiz Thracian Sea (northeastern Aegean Sea) Adriatic Sea Silva et al. (2004) E. Lefkaditou, pers. comm. 0.2371 2.960 M 0.6002 2.6644 F 0.5246 2.7665 M Krstulović Šifner and Vrgoč (2009a) Cephalopod biology and fisheries in Europe: II. Species Accounts | 47 0.3233 2.702 All Montenegro 0.7712 2.4558 M (Adriatic Sea) 1.1185 2.2291 F 0.9407 2.33 All 0.3083 2.797 F 0.2548 2.885 M 0.2836 2.836 All Iskenderun Bay (northeastern 0.0906 3.324 F Levant Sea) 0.2704 2.7902 M 0.5645 2.4281 All Izmir Bay (eastern Aegean Sea) 5.5.3 Ikica et al. (2011) Akyol et al. (2007) Duysak et al. (2008) Maturation and reproduction Sex ratio apparently varies seasonally and with depth, as well as between areas, perhaps indicating geographic variation in the timing of life cycle events, reproductive migrations, and differential survival of the sexes, but also suggesting an incomplete understanding of the life cycle in many areas. Off the Mediterranean French coast and the Gulf of Gabes (Tunisia), males significantly outnumber females, especially during the reproductive season (Mangold-Wirz, 1963a; Ezzeddine-Najai, 1997). In the Adriatic Sea, the overall sex ratio is normally close to 1:1, but males dominate during summer, soon after the spawning season (Krstulović Šifner and Vrgoč, 2009a). Conversely, both commercial and survey trawl data from the Gulf of Cádiz show a clear female dominance in catches throughout the year (Silva et al., 2004). In Portuguese waters, males and females are equally abundant up to 100 m depth, but between 100 and 200 m, females outnumber males (Lourenço et al., 2008). Females outnumber males (1.31:1) at all depths year-round in the eastern Mediterranean (Akyol et al., 2007). Ikica et al. (2011) found a sex ratio close to 1:1 in Montenegrin waters. Weight and size at maturity vary geographically. In the Gulf of Cádiz, the length and weight at maturity (MLm50% and BWm50%) were estimated to be 12 cm (274 g) in females and 7.8 cm (97 g) in males (Silva et al., 2004). The MLm50% was estimated to be 11 cm (females) and 9 cm (males) in Tunisian waters (Ezzeddine-Najai, 1997), and 9.5 cm (females) and 8.5 cm (males) in the Adriatic Sea (Krstulović Šifner and Vrgoč, 2009a). Also in the Adriatic Sea, Ikica et al. (2011) gives estimates of 7.2 cm and 9.5 cm for MLm 50% in females and males, respectively. In the Gulf of Cádiz, the spawning season extends throughout most of the year, although there is little or no spawning during summer (Silva et al., 2004). Most spawning is during February–May, but with a secondary peak in September in southern Portuguese waters (Lourenço et al. 2008) or in October in the Gulf of Cádiz (Silva et al., 2004). Southwestern and central Mediterranean populations have similar spawning seasons, although slightly time-shifted relative to the Atlantic populations: spawning females are found from November to June–July, peaking between February and May in the Gulf of Gabes (Ezzeddine-Najai, 1997) and between January and April in the Adriatic Sea (Krstulović Šifner and Vrgoč, 2009a). In the eastern Mediterranean, the reproductive season is also extended, with two spawning peaks in the Aegean Sea: one in January and the other in June (Akyol et al., 2007). In contrast, in the northwestern Mediterranean, the reproductive season seems to be restricted to the period January–May (Mangold, 1983b). 48 | ICES Cooperative Research Report No. 325 As in other cephalopods, various environmental variables, particularly temperature, influence the reproductive biology of this species. Higher temperatures extend the reproductive period and affect the precocity of sexual development (Ezzeddine-Najai, 1997). Fecundity studies undertaken throughout the distributional range of E. moschata indicate substantial variability in the number of oocytes per female and a relationship with the size of the animal. Mean total fecundities were estimated to be 100–500 oocytes in the western Mediterranean (Mangold, 1983b), 210–459 oocytes (mean = 310 ± 60) in the Adriatic Sea (Krstulović Šifner and Vrgoč, 2009a), 273–2896 oocytes (836 ± 193) in the Aegean Sea (Akyol et al., 2007), and 187–944 oocytes (443 ± 154) in the Gulf of Cádiz (Silva et al., 2004). As in other octopus species, there are usually residual oocytes in the ovaries, especially in more mature females. The observed mean number of residual oocytes in females from the Gulf of Cádiz was 295.73 ± 132.079 (6.6% ± 2.91 of the total number of oocytes). There, the average relative fecundity was estimated to be 1.43 ± 0.36 oocytes g–1 of female total weight. In the Gulf of Cádiz, the mean size of the largest oocytes was 10.90 ± 1.22 mm, with a maximum size of 14.8 mm. The mean size of all the sampled non-residual oocytes was 10.24 ± 1.07 mm (Silva et al., 2004). In the Adriatic Sea, mean oocyte length and width were 9.39 ± 1.99 mm and 2.57 ± 0.72 mm, respectively (Krstulović Šifner and Vrgoč, 2009a). In the Aegean Sea, Akyol et al. (2007) reported an average oocyte length of 6.26 ± 0.10 mm, with a range of 2.6–10.7 mm. In the Gulf of Cádiz, the mean length of fully developed spermatophores was 13.88 ± 1.60 mm (Silva et al., 2004). The maximum and minimum spermatophore lengths were 17.5 and 10.9 mm, respectively, which were found in two males of 240 (100 mm ML), and 98 g (60 mm ML), respectively. In the Aegean Sea, the average number of spermatophores ranged between 6 and 172 (mean = 52 ± 6), with a mean length of 13.66 ± 0.08 mm (range = 7.3–18.3 mm) (Akyol et al., 2007). In the Adriatic Sea, the number of spermatophores was 45–287 (mean = 120 ± 60), with mean length of 17.71 ± 3.27 mm (range = 9–23 mm) (Krstulović Šifner and Vrgoč, 2009a). In the western Mediterranean, the mean number of spermatophores is ca. 106, with lengths (range = 15–20 mm (Mangold-Wirz, 1963a). The number and size of both oocytes and spermatophores depend mainly on the size of the animal. Internal insemination has been confirmed by the presence of sperm sacs in the ovaries of some females. However, the number of females found in that state has been small, indicating that the number of spermatophores that reach the ovary is low and that copulation takes place shortly before spawning (Mangold, 1983b). 5.6 Biological distribution 5.6.1 Habitat Eledone moschata is a coastal species, living on soft sandy and muddy bottoms, occasionally on gravel. It does not seem to live in rocky areas, except possibly when spawning (Gamulin-Brida and Ilijanić, 1972; Mangold, 1983b). It is mainly distributed at depths of 15–200 m in both Mediterranean waters and Iberian waters of the Gulf of Cádiz, where it is most abundant in shallow waters down to 100 m (Gamulin-Brida and Ilijanić, 1972; Salman et al., 1997; Lefkaditou et al., 1998a; Belcari et al., 2002a; Silva et al., 2004). In the northern Adriatic, densities were nearly 700 km –2 at 10–50 m, but decreased to <300 km–2 at 50–100 m and to ca. 30 km–2 at 100–200 m (Krstulović Šifner et al., 2011). In some areas, it is found at greater depths: to 450 m in the Gulf of Cádiz (Silva et al., 2004), 612 m in southern Portuguese waters (Lourenço et al., 2008), and 320 Cephalopod biology and fisheries in Europe: II. Species Accounts | 49 m in the Aegean Sea (Salman et al., 2000). In the western Mediterranean, it is found in water temperatures of 12–23°C and salinities of 36.5–38.5 (Mangold, 1983b). 5.6.2 Migrations In the Mediterranean Sea, E. moschata seems to undergo horizontal migration related to reproduction, moving inshore to spawn (Mangold, 1983b; Mandić and Stjepcević, 1981). According to Mangold (1983b), when not migrating inshore and offshore, E. moschata is a truly sedentary species, but it does not seem to be solitary. In the laboratory, the animals seem to be active at night, but quiescent during the day (Mangold, 1983b). 5.7 Trophic ecology 5.7.1 Prey Eledone moschata preys mainly on crustaceans (Table 5.2). In the Adriatic Sea, there were crustaceans in 65.0% of stomachs that contained food, and fish and cephalopods were present in 37.8 and 21.8% of stomachs, respectively (Krstulović Šifner and Vrgoč, 2009b). That study also showed that the diet of E. moschata varies according to body size. Small animals (<80 mm ML) fed mainly on crustaceans (which represented 69% by weight of prey), and larger ones on both fish (37%) and crustaceans (31%). In Izmir Bay (Aegean Sea), prey was dominated by crustaceans, but also included fish, gastropods, bivalves, and urchins. Differences in stomach fullness were observed between morning and midday periods (Şen and Akyol, 2011). Table 5.2. Prey composition of Eledone moschata, as known from studies in the central and eastern Mediterranean (compiled from Krstulović Šifner and Vroč, 2009b1; Şen and Akyol, 20112). Taxon Species Osteichthyes indet.1,2 Cepolidae Cepola macrophthalma (as C. rubescens) (red bandfish)1 Clupeidae Sardina pilchardus (European pilchard)1 Engraulidae Engraulis encrasicolus (European anchovy)1 Gobiidae Gobius spp.1, indet.1 Merlucciidae Merluccius merluccius (European hake)1 Crustacea indet.2 Decapoda Dendrobranchiata- Penaeus spp.1 Penaeiodea Pleocyemata- Anapagurus laevis1, Munida rugosa1, Paguridae indet.1 Anomura Pleocyemata-Brach- Liocarcinus depurator1, Macropodia longirostris1, Portunus spp.1 yura Pleocyemata-Car- Alpheus glaber1, Macrobrachium sintangense (as Palaemon el- idea egans)1, P. adspersus1, Palaemonidae indet. 1 Amphipoda indet.1 Mysida indet.1 Ostracoda indet.1 Copepoda Ctenocalanus vanus1, indet.1 Cephalopoda Myopsida indet.1 Alloteuthis media1, Loligo vulgaris1, Loliginidae indet.1 50 | ICES Cooperative Research Report No. 325 Octopoda Eledone moschata1, indet.1 Sepioidea Sepietta oweniana1, Sepiolidae indet.1 Gastropoda indet.2 Bivalvia indet.2 Echinodermata Echinoidea 5.7.2 indet.2 Predators Octopod beaks in stomach contents have not always been identified to species level. Clarke (1986) indicated that it was difficult to distinguish lower beaks from the three subfamilies of the Octopodidae, although some species can certainly be separated (e.g. Octopus vulgaris from E. cirrhosa (M. B. Santos, pers. comm.). Nonetheless, this species is known from cephalopod, fish, seal, turtle, and cetacean stomachs (Table 5.3). Table 5.3. Known predators of Eledone moschata in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalop- Common octopus (Octopus vulgaris) Kallianiotis et al. (2001) Bull ray (Pteromylaeus bovinus) Capapé (1977) Smooth-hound (Mustelus mustelus) Saïdi et al. (2009) Osteich- Common dolphinfish (Coryphaena Massutí et al. (1998) thyes hippurus) oda Chondrichthyes Pinnipedia Swordfish (Xiphias gladius) Salman (2004) Monk seal (Monachus monachus) Salman et al. (2001), Pierce et al. (2011) Cetacea Bottlenose dolphin (Tursiops truncatus) Blanco et al. (2001), Poldan (2004) Turtles Loggerhead sea turtle (Caretta Katić (2006) caretta) 5.8 Other ecological aspects 5.8.1 Parasites Hochberg (1983) documents the presence of fungi, ciliates, dicyemids, helminths (including digeneans and cestodes), nematodes, and copepods in Eledone spp. Parasites specifically identified in E. moschata include the sporozoan Aggregata “octopiana”; dicyemids Dicyema moschatum and Dicyemennea eledones; the helminths Scolex p. unilocularis, S. p. quadrilocularis, Acanthobothrium sp., Orygmatoscolex pusillum, Phyllobothrium pusillus, and Nybelinia lingualis; the nematode Ascaris moschata; and the copepod Pennella varians (Hochberg, 1983, pers. comm.). 5.9 Fisheries In the Atlantic (where it is found in the Gulf of Cádiz and along the adjacent Iberian and African coasts), E. moschata is taken as bycatch by the Portuguese and Spanish bottom-trawl fleets, although in many cases it is discarded because of its low commercial value. In Portugal, for example, 80–100% of E. moschata catches taken by the trawl fleets are usually discarded (Moreno et al., 2010). In recent years (1996–2010), annual landings of musky octopus in the main Spanish ports of the Gulf of Cádiz have averaged ca. 100 t (50–230 t), with a peak between January and April. Cephalopod biology and fisheries in Europe: II. Species Accounts | 51 Eledone moschata is commercially important throughout the Mediterranean, where it is fished mainly with bottom trawls. Catches obtained with other gear are of lesser importance (Relini et al., 1999). Its economic importance in many Mediterranean countries reflects its great abundance, particularly along the southern and eastern coasts and in the Adriatic Sea (Belcari et al., 2002a). It is especially abundant in the northern Adriatic, where, in early winter, bottom-trawl yields of up to 53 kg h–1 may be achieved (Manfrin-Piccinetti and Rizzoli, 1984). However, E. moschata is discarded as bycatch by Turkish bottom trawlers because of its poor commercial value (Akyol et al., 2007). Eledone moschata catches are generally pooled with those of E. cirrhosa and O. vulgaris in commercial landings and in Mediterranean fishery statistics (Sánchez and Martín, 1993; Belcari et al., 1998). For a summary of recent FAO statistics on octopod catches in the Mediterranean, see the chapters on E. cirrhosa and O. vulgaris; even when distinguished from landings of O. vulgaris, landings for both Eledone species are pooled in the FAO database. Although E. moschata is a separate category in landings for the Northeast Atlantic, the only record of this species in the FAO database is 1 t landed by Portugal in 2006. 5.10 Future research, needs, and outlook Important topics for future research on the species include stock separation and investigations of spawning sites. Little is known about its ecology. As is the case for other exploited European cephalopods, separate recording of landings statistics would both enhance our understanding of stock status and help facilitate routine stock assessment. Previous taxonomic work (F. G. Hochberg, pers. comm.) suggests that E. moschata is sufficiently different from other Eledone species to warrant being placed in a separate genus. This possibility should be pursued with molecular techniques. 52 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Sepia officinalis Common cuttlefish Cephalopod biology and fisheries in Europe: II. Species Accounts 6 | 53 Sepia officinalis Linnaeus, 1758 Ángel Guerra, Jean-Paul Robin, Antonio Sykes, Drosos Koutsoubas, Patrizia Jereb, Evgenia Lefkaditou, Noussithé Koueta, and A. Louise Allcock Common names Seiche commune (France); Σουπιά [soupia] (Greece); seppia comune (Italy); choco-vulgar, choco (Portugal); sepia común, sepia, choco, jibia (Spain); common cuttlefish (UK) (Figure 6.1). Synonyms Sepia filliouxi Lafont, 1869. Sepia mediterranea Ninni, 1884. 6.1 Geographic distribution The common cuttlefish, Sepia officinalis Linnaeus, 1758, is found in the Northeast Atlantic and throughout the Mediterranean. In the Northeast Atlantic, there are records from the Faroe Bank and south of the Shetland Islands (Stephen, 1944), and strandings of cuttlebones have been reFigure 6.1. Sepia officinalis. Dorsal view. From ported along the south and west coasts of Guerra (1992). Norway as far north as Trondheim (see Nordgård, 1929; Grieg, 1933; Brattegaard and Holthe, 2001). However, these northern records seem related to marked fluctuations in oceanographic conditions that characterize the North Sea, with its occasional important inflows of Atlantic water, causing immigrations of species normally restricted to southern areas. Sepia officinalis has also been found in waters off Sweden (Skagerrak, Kattegat areas) since the early 1900s (e.g. Massy 1909, 1928), but it appears not to be present in the Baltic Sea, except for occasional incursions in its westernmost part (Rexfort and Mutterlose, 2009). It is found in the central and southern North Sea (Figure 6.2), as recent reviews confirm (Gittenberger and Schrieken, 2004; De Heij and Baayen, 2005). It was recorded from all along the Irish coast (Massy, 1928), and records from the east and west Scottish coasts are listed in Stephen (1944), who refers to occasional wanderings of the species in northern areas in years of strong incursions of Atlantic water. It is in the English Channel (e.g. Boletzky, 1983; Lordan et al. 2001a) and extends south to Northwest Africa (e.g. Bas, 1975; Bravo de Laguna, 1989) as far south as the border between Mauritania and Senegal (Ikeda, 1972; Hatanaka, 1979a; Guerra et al., 2001). Sepia officinalis is abundant and widespread throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello 2004; Salman, 2009), including western and central parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the 54 | ICES Cooperative Research Report No. 325 Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak et al., 2008). Old records of the species in the Sea of Marmara exist (Demir, 1952, in Ünsal et al., 1999), although S. officinalis has not been recorded by more recent research carried out in those waters (Katağan et al., 1993; Ünsal et al., 1999). Figure 6.2. Sepia officinalis. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 6.2 Taxonomy 6.2.1 Systematics Cephalopoda – Coleoidea – Decapodiformes – Sepiida – Sepiidae – Sepia. 6.2.2 Type locality Simply given as ”Oceano”. 6.2.3 Type repository Linnean Society of London, Burlington House, Piccadilly, London W1J 0BF, UK. 6.3 Diagnosis 6.3.1 Paralarvae and hatchlings The species has no paralarval stage. Hatchlings (6–9 mm ML) are similar to juveniles and adults, except for some body proportions and some behavioural patterns (Boletzky, 1983). 6.3.2 Juveniles and adults The maximum reliably reported size recorded is probably 45 cm ML (see Remarks), but smaller cuttlefish (25–30 cm ML) are more common. Sepia officinalis has wide fins, Cephalopod biology and fisheries in Europe: II. Species Accounts | 55 which extend anteriorly slightly beyond the mantle margin. The arm suckers are tetraserial. A hectocotylus develops on the left ventral arm of maturing males, which has 6 rows of normal size suckers proximally and 4–9 rows of reduced suckers medially (Figure 6.3a). The tentacular clubs have 5–6 suckers in transverse rows, which vary in size, and 5–6 medial suckers are twice the diameter of the others. There is a swimming keel, but this does not extend proximally beyond the base of the club. The cuttlebone (Figure 6.3b) is oblong; anteriorly, it tapers to a point, and posteriorly, it is bluntly rounded. Its spine is short and pointed and surrounded by a chitinous shield. In adults, the spine is embedded in chitin. A shallow, narrow sulcus is present only on the last loculus and is absent from the striate zone. Anterior striae are shaped either like an inverted “U” or a shallow ”m”. The inner and outer cone limbs are narrow anteriorly, but more broad posteriorly, whereas the lateral limbs are flared ventrolaterally. The background colour of live animals is light brown. There are scattered white spots on the head and dark pigment around the eyes. There are no dorsal eye spots. Arms I–III have a broad, longitudinal brownish band medially, which extends onto the head. There are bold transverse zebra stripes on the dorsal mantle during the breeding season. The fins have a narrow white band along the outer margin and small white spots that are larger towards the junction of the mantle and fins. The fourth arms of mature males have black and white zebra stripes and white arm spots. (Guerra, 1992; Reid et al., 2005). (a) 6.4 Remarks (b) Figure 6.3. Sepia officinalis. (a) hectocot- ylized arm, (b) cuttlebone. From Guerra Morphological and genetic analyses have (1992). shown that S. officinalis Linnaeus, 1758 and S. hierredda Rang, 1837 are different species of the same genus (Guerra et al., 2001). The mantle of S. hierredda is narrower, and both the unmodified arms and the hectocotylized arm are shorter than those of S. officinalis. The number of transverse rows of reduced suckers on the hectocotylus is higher (8–14) in S. hierredda than in S. officinalis (4–9). The striated zone of the cuttlebone of S. officinalis is smaller (41% of ML) than in S. hierredda (47%). The cuttlebone of S. officinalis is slightly acuminate at the anterior end, but very acuminate in S. hierredda. The spine of S. officinalis is usually covered by chitin, especially in adults, whereas the spine of the cuttlebone of S. hierredda is never covered by chitin. Additionally, 13 diagnostic allozyme loci distinguish these species (Guerra et al., 2001). The genus Sepia Linnaeus, 1758 comprises ca. 100 species. Khromov et al. (1998) proposed a subdivision of the genus into six species complexes, although this suggestion has not been widely adopted. Allozyme electrophoresis (Pérez-Losada et al., 1999) of 32 presumptive loci indicated that S. officinalis (assigned to the genus Sepia sensu stricto) was not closely related to its European congeners Sepia elegans and Sepia orbignyana, both placed in Sepia (Rhombosepion) by Khromov (1998). Young S. officinalis can be distinguished from S. orbignyana and S. elegans by their brown, rather than red, skin colour, the shape of the cuttlebone, and the club sucker 56 | ICES Cooperative Research Report No. 325 arrangement (Guerra, 1992). Comprehensive genetic work on microsatellite DNA variation shows that extensive population subdivisions exist in S. officinalis (e.g. Sanjuan et al., 1996; Shaw and Pérez-Losada, 2000; Pérez-Losada et al., 2002). Off the Northwest African coast, the distribution ranges of S. officinalis and S. hierredda overlap. Recent data and information seem to agree on the southern limit of S. officinalis (16–17°N) and the northern limit of S. hierredda (Cap Blanc, 21°N), thus framing the area of overlap (16–21°N; e.g. Guerra et al., 2001; Reid et al., 2005). However, broader areas of overlap were reported earlier (see Ikeda, 1972 and Delgado de Molina Acevedo et al., 1993 for additional details). This resulted in confusion about the maximum size for the species, because of disagreement about the identity of the (at the time) subspecies examined. According to recently given range distribution limits, the maximum size ever recorded for S. officinalis would be 45 cm ML (Delgado de Molina Acevedo et al., 1993; African waters between 21 and 26°N off Sahara), although a maximum size of 49 cm ML was reported for S. officinalis by Ineji (1990), who studied specimens from Mauritanian waters, i.e. the area of overlap. The maximum size ever recorded for S. hierredda is 50 cm (Bakhayokho, 1983; African waters off Senegal). However, maximum sizes recorded for S. officinalis farther north off Portuguese and French coasts are smaller, reported as 36 and 38 cm ML, respectively (J. Pereira and J-P. Robin, pers. comm.). 6.5 Life history Sepia officinalis has a short (1-year) or long (2-year) life cycle, and these two life-cycle modes may arise alternately or simultaneously. Breeding shows one or two seasonal peaks. Hatchlings immediately assume a nektobenthic lifestyle. 6.5.1 Egg and juvenile development Sepia officinalis generally lay eggs in depths less than 30–40 m, attached in clusters to various plants, sessile animals such as tubeworms, or dead structures such as drowned trees, cables, or nets. No parental care has been reported in the species. Egg diameters are 12–14 mm (Boletzky, 1983). The length of embryonic development varies with temperature and ranges from 40–45 d at 20°C to 80–90 d at 15°C (Naef, 1921/1923; Richard, 1971; Boletzky, 1983). Higher temperatures also result in greater rates of oxygen consumption during embryogenesis. Pimentel et al. (2012) recorded an 11-fold difference between oxygen consumption rates of eggs incubated at 13 and 19°C. Hatchling size varies from 6 to 9 mm ML. Hatchlings immediately adopt a nektobenthic lifestyle; they are similar to adults both in morphology and basic behaviour, although the behaviour patterns of adults become more diverse through learnt behaviours (Hanlon and Messenger, 1996). Hatchlings are sufficiently advanced to feed actively within hours of hatching and seem to show innate preferences for shrimp-like prey (Darmaillacq et al., 2004). However, food imprinting has been demonstrated in cuttlefish hatchlings: visual exposure to crabs for 5 h after hatching changes prey preference from shrimp to crabs (Darmaillacq et al., 2006). Such visual learning has also been demonstrated in late embryos just prior to hatching (Darmaillacq et al., 2008). Young cuttlefish can adapt to very low food intake and remain alive with growth rates much lower than normal, allowing animals to survive under unfavourable conditions (Boletzky, 1983). Cephalopod biology and fisheries in Europe: II. Species Accounts 6.5.2 | 57 Growth and lifespan This species lives ca. 2 years (Dunn, 1999a). In the English Channel, all animals appear to overwinter twice before spawning (Boucaud-Camou and Boismery, 1991; BoucaudCamou et al., 1991). In the Bay of Biscay, early-season hatchlings may develop to maturity after a single winter, spawning late in the season, whereas other individuals may spawn early in the season, having overwintered twice (Le Goff and Daguzan, 1991a). Growth is linear in the early part of the life cycle (Domingues et al., 2002), but growth in laboratory culture slows as size increases (Richard, 1971; Pascual, 1978; Forsythe and van Heukelem, 1987; Forsythe et al., 1994; Koueta and Boucaud-Camou, 1999, 2003; Domingues et al., 2001a, 2002, 2003a). Growth patterns differ between the sexes (Boletzky, 1983). Approaching maturation, female cuttlefish growth rate slows much faster than male growth rate (Domingues et al., 2002, 2003a) because they invest more energy in reproduction. Table 6.1. Sepia officinalis. Maximum mantle length (ML) (mm) for females (F) and males (M) in different geographic areas of the Northeast Atlantic and the Mediterranean Sea. Region F M Reference Bay of Biscay 290 350 Le Goff and Daguzan (1991a) Ría de Vigo 235 205 Guerra and Castro (1988) Biscay Gulf 280 Catalan Sea 250 Tyrrhenian Sea 230 Thracian Sea 264 320 Lefkaditou et al. (2007) Izmir Bay (eastern Aegean Sea) 241 324 Onsoy and Salman (2005) Iskenderun Bay (Levant Sea) 200 Santurtún et al. (2003) 300 Mangold-Wirz (1963a) Belcari et al. (2002b) Duysak et al. (2008) Temperature plays a major role in determining both the growth rate and life span of S. officinalis (Richard, 1971; Pascual, 1978; Forsythe et al., 1991, 1994; Domingues et al., 2001a, 2001b, 2002, 2004). Sepia officinalis can be cultured at a wide range of temperatures, and it still grows at temperatures as low as 9.5°C (Richard, 1971). Generally, growth rate increases with increasing temperature, although it appears that growth slows as the upper physiological tolerance limit is approached. For example, Pascual (1978) reported slower growth at 30°C, which is at the upper tolerance limit for the species (Richard, 1971; Domingues, 1999), than at 22°C. Water temperature at hatching (e.g. Bouchaud and Daguzan, 1989, 1990) likely contributes to the variation in growth rate in S. officinalis, (Le Goff and Daguzan, 1991a). Forsythe and van Heukelem (1987) indicate that daily growth in weight declines with increasing size from 5.5% BW d–1 to 3.75% BW d–1. Domingues et al. (2001b) recorded growth rates in hatchlings of 12.4 ± 4.5% BW d–1, declining to 7.3 ± 0.7% BW d–1 after 40 d. Domingues et al. (2003b) measured growth rates during the first 40 d of hatchling life, obtaining values ranging from 2% BW d –1 to 10% BW d–1. Growth rate depended on diet (being faster on a shrimp than on a fish diet) and declined between 25 and 40 d of age in both feeding groups. Baeza-Rojano et al. (2009) found that cuttlefish hatchlings fed with mysids and gammarids grew faster (6.7 ± 0.4 and 5.7 ± 0.9% BW d–1, respectively) than those fed with caprellids (1.6 ± 0.2% BW d −1). For the English Channel stock, Dunn (1999a) fitted von Bertalanffy growth curves to monthly length-frequency data and showed that a strong seasonal growth pattern overlies almost linear growth in length and weight. Growth was fastest between July 58 | ICES Cooperative Research Report No. 325 and October in males (32.7 mm ML month–1), and between August and December in females (25 mm ML month–1). There was no growth in males between October and December, or between April and May. Slowest growth in females (<4 mm ML month– 1) was between December and May (Dunn, 1999a). The fastest monthly growth rate in (post-recruit) males is equivalent to slightly over 1 mm d–1. As the modal size of males in July was 88 mm ML, specific (daily) growth rate during July–October therefore typically ranged from ca. 1.20% in August to 0.57% in October. Similarly, the female growth rate over the peak growth period ranged from 0.67% ML d –1 to 0.39% ML d–1. Length–weight relationships have been published for populations from several areas from the eastern Atlantic and the Mediterranean Sea (Table 6.2). Statolith increments in S. officinalis are difficult to visualize, and initially other hard structures such as the cuttlebone were examined for age determination (Ré and Narciso, 1994; Le Goff et al., 1998). Results from recent rearing experiments have both verified the daily periodicity of statolith rings and indicated that increments in other hard structures such as the cuttlebone, eye lens, and beaks cannot be used for age determination (Bettencourt and Guerra, 2000, 2001). However, in cuttlefish older than 240 d, statolith rings are hardly visible (Bettencourt and Guerra, 2001). Table 6.2. Sepia officinalis. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference English Channel 0.243 2.78 F Dunn (1999a) 0.305 2.64 M 0.264 2.70 F 0.265 2.70 M 0.242 2.74 F 0.264 2.66 M 0.366 2.60 F 0.275 2.69 M 0.069 3.15 F 0.464 2.35 M 0.220 2.773 All Spain, Ría de Vigo Portugal, Ria de Aveiro Portugal, Ria de Sado Adriatic Sea Guerra and Castro (1988) Jorge and Sobral (2004) Serrano (1992) Neves et al. (2009) Manfrin Piccinetti and Giovanardi (1984) Hellenic Seas 0.0064 2.18 F Lefkaditou et al. (2007) 0.0025 2.37 M Izmir Gulf (eastern Aegean) 0.0867 3.1571 All Akyol and Metin (2001) Iskenderun Bay (Levant 0.1082 2.9226 F Duysak et al. (2008) 0.1415 2.7832 M 0.1159 2.8771 All Sea) Challier et al. (2002) applied statolith-ageing techniques to S. officinalis collected in the wild. Age and growth were estimated using statolith increments from juveniles of 5.3– 13 cm ML collected between October and December 2000 in the French part of the English Channel and from August to December in the Bay of Seine. The pattern of juvenile growth seen was consistent with previous studies based on length-frequency distributions (Medhioub, 1986; Dunn, 1999a). Cephalopod biology and fisheries in Europe: II. Species Accounts | 59 Although there is only one spawning season per year (and hence one annual cohort) in the English Channel, Challier et al. (2002) identified several microcohorts, each representing animals hatched in a particular month. Juveniles hatched in late summer grew more slowly than those hatched earlier (1.18 mm ML d–1 in June, 0.69 mm ML d– 1 in July, and 0.46 mm ML d–1 in August) and, at any given age, were smaller than animals of the same age hatched earlier. Although temperature appears to be the most important environmental factor affecting seasonal growth variation, there is high interindividual variation even within microcohorts. Back-calculations from statolith ring number indicated that most cuttlefish hatch during summer, but some hatching takes place throughout the year (Challier et al., 2005). Fitted growth models (both exponential and linear) indicated that the growth rate of prerecruit specimens was significantly faster in 2002 (23–29 mm ML month–1) than in 2000 (14–19 mm ML month–1). The latter growth rate is consistent with that estimated by Medhioub (1986). Growth rates also varied spatially. In the Bay of Seine, they were 0.018 mm ML d–1 in 2000 and 0.0328 mm ML d–1 in 2002, but off the north coast of the English Channel they were 0.0295 mm ML d–1 in 2000 and 0.0294 mm ML d–1 in 2002. These differences could be due to the influence of low salinity and high turbidity in the Bay of Seine and/or density-dependent effects, because density varies between areas (Challier, 2005). Growth rates were directly correlated with the RNA/DNA ratio in muscle (Clarke et al., 1989; Castro and Lee, 1994; Koueta et al., 2000; Sykes et al., 2004). The RNA content of tissues typically increased with feeding and growth (Melzner et al., 2005). 6.5.3 Maturation and reproduction Dunn (1999a) found that the overall sex ratio of cuttlefish in commercial trawl catches was not significantly different from 1:1. Common cuttlefish attain sexual maturity at a wide range of sizes. In the English Channel, 4% of males matured at 8.1–9.1 cm ML in August at an age of ca. 1 year. Of the remaining males, the first matured at 11.4 cm ML, MLm50% was reached at 14.6 cm ML, and all were mature at 17.0 cm ML. In females, the smallest sexually mature individuals were 14.2 cm ML, MLm50% was 16.4 cm ML, and all females were mature at 23.0 cm ML (Dunn, 1999a). In the Mediterranean Sea, males mature as small as 6–8 cm ML, although males >10 cm ML may still be immature. Females may become fully mature at sizes of 11–25 cm ML (Mangold-Wirz, 1963a; Boletzky, 1983). Off the coast of Africa, first maturity is between 12 and 14 cm ML in males and at 14 cm in females (Hatanaka, 1979b). Early gonad growth (before attainment of maturity) is linked to somatic growth and is therefore temperature-dependent. Light and, more particularly, short wavelength light (blue to blue-green), has a decelerating effect on gonad maturation via the hormonal control of optic glands, whereas in mature animals, it stimulates mating and spawning. High temperatures and weak light intensities / short days result in fast growth rates and gonad maturation. In shallow water under summer conditions of high temperature, high light intensity, and long day length, growth accelerates and maturation decelerates. In deeper water under winter conditions, growth is slow because of the low temperature, but maturation is largely unaffected (rather than accelerated) (Richard, 1966, 1971, 1975; Boletzky, 1983). At maturity, the reproductive organs may represent up to 16% of body weight in females and a maximum of 5% of body weight in males (Boletzky, 1983). Males may carry up to 1400 spermatophores (Mangold-Wirz, 1963a). Estimates of fecundity for 60 | ICES Cooperative Research Report No. 325 females vary widely, although some of the variation probably relates to how fecundity is measured. According to Mangold-Wirz (1963a), females lay 150–4000 eggs, depending on their size. Laptikhovsky et al. (2003) reports that potential fecundity (PF) of advanced maturing and mature prespawning S. officinalis in the Aegean Sea varies from 3700 to 8000 (mean 5871) oocytes, whereas the number of large yolky oocytes increases with ML from 130 to 839. Further, spawning females typically have a PF of 1000–3000 fewer eggs than pre-spawning females. This provides evidence that intermittent spawning, which does take place in captivity (Boletzky, 1987a), is a normal process in natural habitats. Female common cuttlefish may release a number of eggs equivalent to ca. 50% of PF during spawning. The reproductive behaviour of this species is well known (Hanlon and Messenger, 1996). The species has elaborate courtship behaviour, during which spermatophores are transferred to a special pouch under the buccal mass of the female (Boletzky, 1983). A single pair can mate several times in succession, with the female sometimes laying between matings. Under culture conditions, temporary mate guarding by the male has been observed, but when guarding relaxes, other mature males can copulate with the female, providing evidence of promiscuity, at least in the laboratory. Sperm competition may be relevant in this species (Hanlon et al., 1999), and microsatellite DNA markers provide evidence of multiple paternity (Á. Guerra, pers. comm.). Unbalanced sex ratios are seen in mating and egg-laying areas along the west coast of Normandy. Zatylny (2000) proposed that this was linked to sperm storage. Sepia officinalis is an intermittent terminal spawner sensu Rocha et al. (2001). This reproductive pattern is characterized by “group synchronous ovulation and monocyclic spawning”. Although egg laying is in separate batches and the spawning period tends to be relatively long, somatic growth does not generally take place between spawning events (Rocha et al., 2001). Sepia officinalis spawns mainly in spring and summer in the western Mediterranean and Gulf of Tunis, but winter spawning has also been observed (Mangold-Wirz, 1963a; Najaï, 1983). Spawning extends from early spring to late summer in southern and central Portugal and the Atlantic and Mediterranean coasts of southern Spain, with a spawning peak in June and July (Villa, 1998; Tirado et al., 2003; Jorge and Sobral, 2004). A similar spawning season is found northwest of the Iberian Peninsula, but winter spawning has also been recorded there (Guerra and Castro, 1988). In the Bay of Biscay and the Gulf of Morbihan, spawning takes place from mid-March to late June (Le Goff and Daguzan, 1991a). Along both the north and the south coasts of the English Channel, the spawning season of S. officinalis extends from February to July (Dunn, 1999a; Royer, 2002; Royer et al., 2006; Wang et al., 2003). Environmental factors (much milder winter conditions in some areas) probably account for most of the variation observed in S. officinalis spawning times (Boletzky, 1983). Restricted food supply in early life may delay maturation and extend the lifespan in this species (Boletzky, 1979a). The length of time spent under optimal conditions in the early juvenile phase (inshore spring and summer conditions) determines whether an individual becomes sexually mature during the first winter. The first females to arrive at the spawning grounds in many areas have overwintered twice and are ca. 18 months old (Boletzky, 1983). Later in spring and up to late summer, mature females of smaller size appear in the shallower waters and spawn. These are only 14–16 months old and could be offspring of large animals that spawned early the previous year. This is the basis of a hypothesis of a cycle of alternating shorter and longer generations. One- and two-year-old breeders have been observed in southern Brittany at the same time; the spawning season for Cephalopod biology and fisheries in Europe: II. Species Accounts | 61 these two groups overlaps, and they most likely interbreed (Le Goff and Daguzan, 1991b). 6.5.4 Natural mortality Females die shortly after spawning, and mass mortality has been observed on the French and Spanish Atlantic coasts (Richard, 1971; J-P. Robin, pers. comm.; Á. Guerra, pers. comm.), but nothing of comparable intensity has been reported from the Mediterranean (Boletzky, 1983). Other causes of natural mortality include predation and disease. 6.6 Biological distribution 6.6.1 Habitat Sepia officinalis is a neritic, nektobenthic, or demersal species found on the continental shelf and is particularly common on sandy and muddy substrata covered by algae and marine grasses (Zostera and Posidonia). Its depth distribution extends from subtidal waters to 200 m. Individuals are most abundant in the upper 100 m, with large animals found at greater depth (Guerra, 1992; Reid et al., 2005). Shell morphology limits its depth range; shells of large animals implode between 150 and 200 m, whereas advanced embryonic specimens and newly hatched animals implode between 50 and 100 m (Ward and Boletzky, 1984). Sepia officinalis is relatively tolerant of variations in salinity. Animals have been observed in coastal lagoons in the Mediterranean at a salinity of 27 (Mangold-Wirz, 1963a). Observations from the western Mediterranean and the Northeast Atlantic have shown that juveniles and adults can survive for some time at salinities of 18 ± 2 if slowly acclimatized (Boletzky, 1983; Guerra and Castro, 1988). In culture, some embryos of S. officinalis from eggs collected off the southwest coast of the Netherlands hatched at a salinity of 26.5, but there was no hatching below 23.9; below 22.4, embryos with morphological malformations were found (Paulij et al., 1990a). The temperature limits of the species range from 10 to 30°C. At temperatures <10°C, individual cuttlefish do not feed, remain inactive, and die within a couple of days (Richard, 1971; Bettencourt, 2000). Hatchlings and young S. officinalis have been successfully cultured in tanks with an open seawater system in which the temperature reached 30°C (Domingues et al., 2001b); indeed, the species lives in the lagoon system of the Ria Formosa (southern Portugal) where temperatures reach 27 ± 3°C in summer (Domingues et al., 2002). Oxygen affinity in S. officinalis, expressed as P50 (partial pressure of gas at which the blood remains 50% saturated), increased as a function of temperature from 12 mm Hg at 5°C to near 38 at 17°C. This is an indication that the species does not have the ability to accommodate large temperature ranges in its natural habitat (Brix et al., 1994). Recent findings by Melzner et al. (2006, 2007) support the hypothesis that the upper thermal tolerance limit is due to oxygen limitation. Moreover, Johansen et al. (1982) concluded that the common cuttlefish is not very tolerant of low oxygen concentrations. This may explain the variations in densities between the Northwest African coast and the northern Benguela, where low oxygen concentrations are common as a consequence of shallow-water eutrophication (Guerra and Sánchez, 1985). Analysis of a time-series of 18 years of landings per unit effort of cuttlefish in southwestern Spain indicates that the abundance of S. officinalis does not correlate with rainfall, river discharge, or sea surface temperature (Sobrino et al., 2002). The species is 62 | ICES Cooperative Research Report No. 325 apparently able to endure changing environments, not only during its adult phase, but also during the early juvenile stage (Sobrino et al., 2002). However, strong precipitation had a negative influence on cuttlefish abundance in the Ria de Aveiro (central Portugal) and, together, high solar radiation, air temperature, near-bottom salinity, and good water clarity seemed to influence catches of the species positively (Jorge and Sobral, 2004). 6.6.2 Migrations Seasonal migrations between shallow and deeper water are a well-known ecological feature of S. officinalis. In the western Mediterranean, they migrate inshore in spring and summer to mating/spawning grounds and offshore in autumn to to the winter feeding grounds, although not all animals migrate at the same time, size, and age (Mangold, 1966). The migrations are over different distances, from a few dozen to several hundred nautical miles, and represent an important displacement of biomass, something that has also been observed elsewhere (Richard, 1971; Najaï, 1983; Guerra and Castro, 1988; Boucaud-Camou and Boismery, 1991; Coelho and Martins, 1991; Le Goff and Daguzan, 1991b; Jorge and Sobral, 2004). The autumn/winter offshore migration in the English Channel is mainly influenced by cooling of littoral waters (BoucaudCamou and Boismery, 1991). However, day-length reduction and decreased light intensity, which are other factors influencing maturation and spawning (Boletzky, 1983; Boucaud-Camou et al., 1991), are also involved in this migration. Hence, the relatively deep milder waters at the central axis of the Channel seem to constitute the common hibernation area to all cuttlefish in the English Channel, which they leave at the end of winter. Spring inshore displacements are mainly attributable to an increase in temperature in littoral waters. These displacements were documented by tagging experiments (Boucaud-Camou and Boismery, 1991), but this spatial and temporal pattern is also supported by an analysis of georeferenced data from both sides of the English Channel (Dunn, 1999a; Denis and Robin, 2001; Royer, 2002; Wang et al., 2003; Royer et al., 2006). In the western part of the English Channel and the southern part of the Celtic Sea, local abundance is positively correlated with sea surface temperature, with cuttlefish expanding their distribution farther north in the spawning seasons in warm years. The centre of high abundance in offshore deep water shifts north in warm winters and south in cool winters (Wang et al., 2003). 6.7 Trophic ecology 6.7.1 Prey Sepia officinalis is a trophic opportunist: its diet includes crustaceans, bony fish, molluscs, polychaetes, and nemertean worms (Nixon, 1987; Castro and Guerra, 1990; Pinczon du Sel et al., 2000). The main crustacean prey items are mysids, shrimps, prawns, and crabs, but S. officinalis also feeds on amphipods, isopods, and ostracods. It feeds on gobies, sandeels, whiting, and wrasses, but can also prey on some flatfish. The most common cephalopod prey are various sepiolid and sepiid species (Table 6.3). Large cuttlefish are also cannibalistic, capturing and eating smaller individuals. Amphipods, mysids, caridean shrimps, and other small crustaceans, which commonly swarm in large schools just above the bottom, are important in the diet of juvenile cuttlefish (Nixon and Mangold, 1998; Blanc et al., 1998). Cannibalism begins during the juvenile stage (ML < 3.0 cm) (Henry and Boucaud-Camou, 1991). Other small-sized items found in the stomach of cuttlefish, such as bryozoans, foraminiferans, bivalve molluscs, insects, and algae, should be regarded with caution, because they could be the prey of prey, or accidentally ingested (Castro and Guerra, 1990). Cephalopod biology and fisheries in Europe: II. Species Accounts | 63 Table 6.3. Prey composition of Sepia officinalis, as known from studies in the Mediterranean Sea and the Northeast Atlantic (compiled from Najaï and Ktari, 19791; Castro and Guerra, 19892; Le Mao, 19853; Castro and Guerra, 19904; Henry and Boucaud-Camou, 19915 Pinczon du Sel and Daguzan, 19976; Blanc et al., 19987; Nixon and Mangold, 19988; Pinczon du Sel et al., 20009; Vafidis et al., 200910). Taxon Species Osteichthyes Ammodytidae Ammodytes tobianus (small sandeel)4, indet.4,8 Anguillidae Anguilla anguilla (European eel)6,8 Atherinidae Atherina presbyter (sand smelt)3,8 Belonidae Belone belone (garfish)3 Bothidae Arnoglossus laterna (Mediterranean scaldfish)2, Arnoglossus spp.2 Callionymidae Callionymus lyra (dragonet)3,4, indet.8 Carangidae Trachurus trachurus (Atlantic horse mackerel)8 Clupeidae indet.3 Gadidae Trisopterus luscus (pouting)2, Trisopterus spp.4,6, indet.3 Gobiidae Aphia minuta (transparent goby)4, Deltentosteus quadrimaculatus (four-spotted goby)4, Gobius niger (black goby)4, G. paganellus (rock goby)4, Gobius spp.2,4,7, Lesueurigobius friesii (Fries's goby)2,4, Pomatoschistus minutus (sand goby)4, P. pictus (painted goby)4, Pomatoschistus spp.3,4, indet.3,6,8 Gobiesocidae Lepadogaster spp.4 Labridae Symphodus spp.4, indet.3,4,6,8 Moronidae Dicentrarchus labrax (European seabass)3 Mullidae Mullus surmuletus (striped red mullet)8 Pleuronecti- indet.3 dae Soleidae Buglossidium luteum (solenette)4, indet.8 Sparidae Spondyliosoma cantharus (black seabream)3 Syngnathidae Syngnathus acus3, S. typhle (broadnosed pipefish)4, Sygnathus spp.3,4,6,7, indet.4 Trachinidae Echiichthys vipera (as Trachinus vipera) (lesser weaver)4 Crustacea Decapoda Dendrobran- Penaeus spp.1 chiata-Penaeiodea Macrura rep- Nephrops spp.8 tantiaAstacidea Pleocyemata- Galatheidae indet.4, Pagurus bernhardus3, Paguridae indet.4, Pisidia Anomura longicornis2,3,4, Porcelana platycheles2,4, Porcellanidae indet.2 Pleocyemata- indet.7 Axiidea Pleocyemata- Asthenognathus atlanticus4, Atelecyclus undecimdentatus2,4, Carcinus Brachyura maenas3,4,6,7,8, Ebalia spp.8, Galathea spp.8, Inachus spp.3,4, Liocarcinus corrugatus2, L. depurator2,3,4,6,8, L. marmoreus4, L. navigator7, Liocarcinus spp.3,4, Necora puber (as L. puber)3,6,8, Pilumnus spinifer4, Macropodia rostrata3, Macropodia spp.3,8, Maja squinado3,8, Majidae indet.3,4, Polybius henslowii2, Portunidae indet.2,3,4, indet.2,6,7,8,9,10 64 | ICES Cooperative Research Report No. 325 Pleocyemata- Crangon crangon2,3,4,6, (as C. vulgaris)5,8, Crangonidae indet.4, Palae- Caridea mon adspersus2,4,7, P. serratus2, Palaemon spp.4,6,7, Palaemonidae indet.4, Philocheras fasciatus (as C. fasciatus)5,8, Processa edulis4, indet.2 Mysida indet.3,8,9,10 Ostracoda indet.1 Amphipoda Ampelisca brevicornis7, A. spinipes3, Ampelisca spp.3, Caprelloidea indet.3,4, Dexamine spinosa7, Echinogammarus marinus7, Ericthonius spp.3, Gammaridea indet.3,4, Phtisica marina7, indet.1,3,4,7,9,10 Isopoda Sphaeroma spp.1, indet.7 Copepoda indet.1 Cephalopoda Sepioidea Sepia elegans4, S. officinalis2,3,4,6,8, Sepia spp.4, Sepiola spp.2, indet.1 Gastropoda Thecosomata indet.1 Bivalvia Lamellibranchiata indet.1, Mytilus edulis3, Polititapes virgineus3 Polychaeta Marphysa spp.3, Nereidae indet.3, indet.1,9,10 Nemertea indet.1 Algae Cymodocea spp.1, Posidonia oceanica2, Zostera marina2, indet.1,8 Significant ontogenetic changes in the diet of this species have been found, with the progressive replacement of crustaceans by fish (Castro and Guerra, 1990). The natural diet of young cuttlefish (<8.5 cm ML) captured from the wild was mainly crustaceans (89%), with fish constituting only 4.6% (Blanc et al., 1998). Ontogenetic changes in the size of prey taken have also been well documented (Blanc et al., 1999; Blanc and Daguzan, 2000). Small specimens (ML <6.5 cm) of S. officinalis and adult S. elegans (ML 4.5–6.5 cm) consume similar prey, although in different proportions, suggesting there may be trophic competition between the two species at that size range (Castro and Guerra, 1990). Prey remains found in cephalopod stomachs tend to be difficult to identify visually because they are chopped into small pieces by the beaks during ingestion. Molecular prey identification currently looks to be the most promising solution (Roura et al., 2012). Previous work used antisera raised to prey proteins, and a study by Kear and Boyle (1992) used S. officinalis as an experimental animal, showing that, when fed on Euphausia superba, prey antigenicity in the digestive tract persisted for up to 8 h. Despite the small size of the mouth, cuttlefish can seize relatively large prey with their prehensile arms and tentacles. This, together with voracity, versatile feeding habit, and highly evolved visual and sensory systems, allows them to occupy a broad trophic niche. Further, migrations enable S. officinalis populations to exploit the temporal and spatial variability of productive systems and fluctuating populations of prey (Rodhouse and Nigmatullin, 1996). The tentacles of S. officinalis can reach prey in less than 15 ms. Prey handling is rapid, and neurotoxins secreted by the posterior salivary glands paralyse the prey within 10 s of capture (Hanlon and Messenger, 1996). External digestion does not appear to take place, and (when feeding on crustaceans) many pieces of exoskeleton are ingested (Guerra et al., 1988). Several studies have investigated the diel pattern of feeding, showing that most feeding is during darkness (Castro and Guerra, 1989; Pinczon du Sel et al., 2000; Quintela and Andrade, 2002). Hence, prey detection in S. officinalis may involve light emitted from their light organs or may even be facilitated by dinoflagellate luminescence (Fleisher and Case, 1995). Cephalopod biology and fisheries in Europe: II. Species Accounts | 65 The trophic position of S. officinalis in an estuarine community (a Zostera meadow in San Simón Inlet, Ría de Vigo) was investigated using 13C and 15N stable isotope signatures from muscle tissue of S. officinalis and sympatric organisms (Filgueira and Castro, 2002). Surprisingly, small cuttlefish appeared to be at a higher trophic level. This may be explained by the complex migrations and life cycle of the species. The smallest mature animals used in this study (60 mm ML for males and 80 mm ML for females) might never have left San Simón Inlet, their isotopic composition representing the local foodweb. The largest animals were probably coming back from deeper water and had an isotopic composition that did not result from the local foodweb. As the metabolic rate of large animals is slower than that of smaller ones, isotopic signals from deeper water will also persist longer in their tissues. Using more tissues with different nitrogen and carbon turnover rates can, therefore, be useful (e.g. Hobson and Cherel, 2006). 6.7.2 Predators The first evidence of predation on eggs of S. officinalis came from the Ría de Vigo (northwestern Spain) at a depth of 10 m in late April 2010. A tompot blenny (Parablennius gattorugine) attacked a black ink-stained cuttlefish egg mass in a late stage of development that had been laid on pod weed (Halydris siliquosa) (Guerra and González, 2011). Recently, various crab species have also been recorded as preying upon S. officinalis eggs (Á. Guerra, pers. comm.). Juvenile and adult S. officinalis are preyed upon by a wide range of fish species, and adult S. officinalis are taken by several species of marine mammal (Table 6.4). Hatchling and juvenile common cuttlefish are taken by Serranus cabrilla in Posidonia grass areas of the Mediterranean (Hanlon and Messenger, 1988). Pollack (Pollachius pollachius) exert great predatory pressure on young cuttlefish in French waters of northern Brittany (Le Mao, 1985). In the Bay of Biscay, Velasco et al. (2001) found S. officinalis in the stomach contents of Pagellus acarne, Aspitrigla cuculus, A. obscura, Lophius piscatorius, L. budegassa, Trisopterus luscus, Lepidorhombus whiffiagonis, and L. boscii. In Morbihan Bay, young cuttlefish have been found in the stomach contents of Dicentrarchus labrax, Labrus bergylta, Spondyliosoma cantharus, and Conger conger (Blanc and Daguzan, 1999). Elsewhere, S. officinalis has been recorded from the stomachs of numerous teleosts and cartilaginous fish species (Table 6.4). Two pinnipeds (Atlantic grey and monk seals) and three dolphin species (bottlenose, Risso's, and oceanic striped) are known to feed on S. officinalis (Table 6.4). Additionally, some remains identified as Sepia spp. or simply Sepiidae have been observed in the harbour porpoise and in bottlenose, common, and oceanic striped dolphins (Santos, 1998). 66 | ICES Cooperative Research Report No. 325 Table 6.4. Known predators of Sepia officinalis in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Chondrich- Black-mouthed dogfish (Galeus Velasco et al. (2001) thyes melastomus) Blainville's dogfish (Squalus Martinho et al. (2012) blainville) Bluespotted seabream (Pagrus Hamida et al. (2010) caeruleostictus) Blue shark (Prionace glauca) Clarke and Stevens (1974) Bull ray (Pteromylaeus bovineus) Capapé (1977) Lesser spotted dogfish (Scyliorhi- Morte et al. (1997), Kabasakal (2002), nus canicula) Martinho et al. (2012) Pelagic stingray (Pteroplatytry- Lipej et al. (2013) gon violacae) Smooth-hound (Mustelus mus- Morte et al. (1997), Saïdi et al. (2009) telus) Osteichthyes Ballan wrasse (Labrus bergylta) Blanc and Daguzan (1999) Bib (Trisopterus luscus) Velasco et al. (2001) Black seabream (Spondylio- Blanc and Daguzan (1999) soma cantharus) Black-bellied angler (Lophius Velasco et al. (2001) budegassa) Brill (Scophthalmus rhombus) Vinagre et al. (2011) Comber (Serranus cabrilla) Hanlon and Messenger (1988) Common pandora (Pagellus Rosecchi (1983) erythrinus) Conger eel (Conger conger) Blanc and Daguzan (1999) Dusky grouper (Epinephelus Reñones et al. (2002) marginatus) European barracuda (Sphy- Kalogirou et al. (2012) raena sphyraena) European hake (Merluccius Larrañeta (1970), Velasco et al. (2001) merluccius) European seabass (Dicentrar- Blanc and Daguzan (1999) chus labrax) Fourspot megrim (Lepidorhom- Velasco et al. (2001), Teixeira et al. bus boscii) (2010) Greater amberjack (Seriola Matallanas et al. (1995) dumerili) Longfin gurnard (Aspitrigla ob- Velasco et al. (2001) scurus) Megrim (Lepidorhombus whiffi- Velasco et al. (2001) agonis) Monkfish (Lophius piscatorius) Daly et al. (2001), Velasco et al. (2001) Pollack (Pollachius pollachius) Le Mao (1985) Red gurnard (Aspitrigla cuculus) Velasco et al. (2001) Silver-cheeked toadfish (Lago- Kalogirou (2011) cephalus sceleratus) Cephalopod biology and fisheries in Europe: II. Species Accounts | 67 Spanish bream (Pagellus Velasco et al. (2001), Fehri-Bedoui et acarne) al. (2009) Spotted flounder (Citharus lin- Teixeira et al. (2010) guatula) Swordfish (Xiphias gladius) Hernández-García (1995), Salman (2004) Turbot (Scophthalmus maximus) Vinagre et al. (2011) Twaite shad (Alosa fallax) Assis et al. (1992) Yellow-mouth barracuda (Sphy- Kalogirou et al. (2012) raena viridensis) Yellow-stripe barracuda (Sphy- Kalogirou et al. (2012) raena chrysotaenia) Pinnipedia Atlantic grey seal (Halichoerus Ridoux et al. (2007) grypus) Monk seal (Monachus mona- Salman et al. (2001) chus) Cetacea Bottlenose dolphin (Tursiops Cockcroft and Ross (1990), Poldan truncatus) (2004), Dos Santos et al. (2007) Risso’s dolphin (Grampus Clarke and Pascoe (1985), Blanco et griseus) al. (2006), Bearzi et al. (2011) Oceanic striped dolphin (Sten- Spitz et al. (2006) ella coeruleoalba) 6.8 Other ecological aspects 6.8.1 Parasites Various parasites, including protistans and metazoans, such as fungi, coccidians, microsporidians, ciliates, dicyemids, diageneans, cestodes, nematodes, brachyurans, copepods, and isopods, are known in juvenile and adult S. officinalis, but most of them do not appear to be very important as mortality factors at pre-reproductive stages. For example, the copepod Metaxymolgus longicaudata is sometimes associated with this cuttlefish, but its effects have not been elucidated (Ho, 1983). Massive digestive tract infections with Aggregata eberthi might result in a decrease or malfunction of absorption enzymes (Gestal et al., 2002a, b). Sexual stages of the coccidian Aggregata eberthi are found in the digestive tract of S. officinalis, and asexual stages infect the digestive tract of crustaceans. Transmission is likely via consumption. The virus-like particles found in the stomach epithelium of wild S. officinalis have a structure similar to vertebrate ”retroviruses” (Hanlon and Forsythe, 1990). Cultured in the laboratory, this species showed susceptibility to a highly virulent systemic infection by bacteria (Pseudomonas and Vibrio), which does not appear to be related to external injury (Hanlon and Forsythe, 1990). To date, few interspecific associations (excluding parasitism) have been reported for this species. Bacterial populations associated with S. officinalis have been localized, mainly in the accessory nidamental glands, the renal appendages, and the shell epithelium. The accessory nidamental glands are coloured intense orange-red in mature females, and this colour is due to carotenoid pigments, which are found in symbiotic bacteria (Van den Branden et al., 1980). Five symbiotic bacterial taxa (Agrobacterium, Roseobacter, Rhodobium-Xanthobacter, Sporichthya, and Clostridium) were identified in the tubules of the accessory nidamental glands, and three taxa of Pseudomonodaceae were located in the renal appendages and the shell epithelium. All these bacteria, except 68 | ICES Cooperative Research Report No. 325 Gram-positive ones, were also present in embryos, suggesting vertical transmission, i.e. maternal transmission at egg stage (Grigioni and Boucher-Rodoni, 2002). 6.8.2 Contaminants Studies on the concentration and distribution of heavy metals in tissues of S. officinalis have shown high levels of bioaccumulation (Miramand and Bentley, 1992; Bustamante et al., 2004, 2006; Miramand et al., 2006; Lacoue-Labarthe et al., 2008a, b, 2009, 2010). Culture experiments at different stages of the life cycle of S. officinalis using zinc and cadmium tracers with seawater, sediments, and food as uptake pathways showed that food is the likely primary route for bioaccumulation, and that the digestive gland plays a major role in the subsequent storage and presumed detoxification of these elements, regardless of the uptake pathway (Bustamante et al., 2002a, b). Bioaccumulation rates of silver and cadmium during early development have been observed to differ (Lacoue-Labarthe et al., 2008a). Juvenile physiology (digestive, immune and nervous systems) can be disturbed by heavy metals (e.g. silver, cadmium, copper) and some pharmaceutical residuals (Le Bihan et al., 2004), impacting behaviour and negatively affecting embryo growth and hatchling survival (Le Bihan et al., 2004; Lacoue-Labarthe et al., 2010; Di Poi et al., 2013). Ecotoxicological studies using bioassays from isolated digestive gland cells demonstrated that some heavy metals (copper, zinc, and silver) disrupt enzymatic systems (Le Bihan et al., 2004). Malformed common cuttlefish caught in the Bay of Arcachon could be a product of the teratogenic effects of the antifouling compound tributyltin (TBT) (Schipp and Boletzky, 1998). 6.8.3 Behaviour The seasonal migrations between shallow and deeper waters bring S. officinalis into contact with various types of soft and rocky bottoms. The ability of small juveniles to attach themselves to a hard substratum may be important because it allows them to withstand strong water movement without being carried away. These animals are able to bury themselves in soft bottoms, and the behavioural pattern of this sand covering is well established at hatching (Boletzky, 1983). Sepia officinalis has a considerable repertoire of defensive strategies involving a large number of chromatic, textural, and postural components (Hanlon and Messenger, 1996). Sepia officinalis does not form shoals, neither in the wild or in the laboratory (Guerra, 2006). However, in culture, individuals tolerate one another except under extreme food deprivation. This tolerance is higher in young animals than in subadults and adults (Hanlon and Messenger, 1996). A feeding hierarchy first appearing after 4 months, which stabilizes after 5 months, has been found in the species (Warnke, 1994). Captiverearing experiments indicated that the behaviour of S. officinalis is strongly affected by aquarium conditions and suggested that the species is probably semi-solitary under natural conditions (Boal et al., 1999). 6.9 Fisheries Sepia officinalis is an important species for the commercial fisheries of many countries. In data reported by FAO, most cuttlefish landings for the Northeast Atlantic area are grouped under “Cuttlefish and bobtail squid nei”, with only a small proportion distinguished as common cuttlefish. However, both these categories likely consist mainly of S. officinalis. Cuttlefish landings from this area increased rapidly after the mid-1980s, rising from a (then) high of 12 000 t to almost 31 000 t in 2004. FAO values for the Mediterranean indicate that common cuttlefish landings have been relatively stable Cephalopod biology and fisheries in Europe: II. Species Accounts | 69 over the past two decades (typically ca. 10 000 t annually), but again a large proportion (≥50%) of landings of Sepiidae are grouped under “Cuttlefish and bobtail squid nei”, so the true figures for S. officinalis are uncertain. The mean annual catch of this species in Europe during the years 1993–2003 was ca. 41 000 t, taken more or less equally from the Atlantic and the Mediterranean (Hastie et al., 2009a). In European waters, French and Italian fisheries make the biggest landings. The main areas of capture of cuttlefish are Italian waters, the English Channel, and the Bay of Biscay. The UK, Greece, Spain, and Portugal are also important European producers, as are Tunisia, Turkey, and Morocco outside of Europe. In northern areas (English Channel and adjacent waters), S. officinalis is usually the only cuttlefish species landed, whereas in southern fisheries, official statistics can include other Sepiidae (mainly S. elegans and S. orbignyana and farther south – Mauritania, Senegal – S. hierredda). Northern fisheries are mainly based on trawling (Dunn, 1999a, b; Denis and Robin, 2001), although trap fishing can be significant during the inshore spawning season. Farther south, cuttlefish are caught by a variety of artisanal gears, including gillnets, trammelnets, traps, and jigs. Recruitment is defined as the renewal of a stock via young classes that enter the fishery, so it depends on the size selectivity of the fishery and on the life cycle of the exploited population. In S. officinalis, both factors vary widely across the distribution range. Trawlers that land the majority of cuttlefish in many regions operate on both inshore and offshore fishing grounds and take both juvenile and adult specimens, whereas traps catch mainly spawning adults in inshore waters. In the English Channel fishery, the length structure of trawler landings suggest that juveniles enter the fishery in autumn and spring; there are two peaks for each annual cohort, related to the migration cycle (Royer et al., 2006). However, a more detailed analysis of age-at-recruitment (Challier et al., 2005) showed that the second peak was not constant and that age-at-recruitment was similar throughout the year (3–4 months). UK beam trawlers operating offshore probably catch only larger and older cuttlefish, but there is no biological sampling available for that fleet. Studies have shown considerable genetic structuring throughout the range of S. officinalis (e.g. Pérez-Losada et al., 1999, 2002, 2007; Wolfram et al., 2006; Turan and Yaglioglu, 2010). This is generally best explained by a model of isolation by distance, although some contemporary physical barriers to gene flow do exist, including the Almería–Oran front. High population structuring favours treating local populations, like that exploited by inshore small-scale fisheries in San Simon Inlet, as discrete stocks. Indeed, mtDNA evidence of population structuring in Turkish coastal waters has been further supported by studies on body morphometry and cuttlebone chemistry, revealing four discrete stocks in Antalya and Iskenderun bays, Izmir Bay in the Aegean Sea, and the Sea of Marmara (Turan and Yaglioglu, 2010). However, genetic differences are unclear in northern fisheries (Wolfram et al., 2006). Spatial distribution on wintering grounds suggests that there can be exchanges between the Bay of Biscay and the English Channel (Wang et al., 2003). The rationale for defining the English Channel stock as a management unit relies on the fact that catch per unit effort is lower in adjacent waters (Royer et al., 2006). Also, the life cycle is 2 years there, but can be shorter in the Bay of Biscay. There is currently no routine stock assessment of this species in Europe. However, several exercises have been carried out to test the feasibility of different methods and to indicate the exploitation status of past cohorts. 70 | ICES Cooperative Research Report No. 325 In the S. officinalis gillnet fishery in San Simón Inlet during 1997–2001, the estimated instantaneous rate of natural mortality (M) over a 6-month period (November–April) was in the range 2.27–3.38, the mean being 2.70 (Outeiral, 2002; F. Rocha, pers. comm.; Á. Guerra, pers. comm.). These values were estimated by different methods based on data for the Galician Rías from Guerra and Castro (1988) and Bettencourt (2000) and are similar to those calculated by Emam (1994) for the exploited population of Sepia prashadi in the Gulf of Suez. The mean value of M estimated for S. officinalis in San Simón Inlet corresponds to an annual mortality rate (A) of ca. 93% of the total number of individuals of a given population, which is very high, and reflects the known catastrophic post-spawning mortality. The first model of population abundance and exploitation rate applied to S. officinalis was developed in the Bay of Biscay (Gi Jeon, 1982). That exercise used virtual population analysis (VPA), with a monthly time-scale for catches and two age groups (according to the bimodal length structure). Low exploitation rates were obtained, but it is questionable whether the authors had access to sufficiently comprehensive fishery statistics in the years 1978–1979. In the English Channel, Leslie–De Lury depletion methods were applied by Dunn (1999b) "assuming a UK stock" (French catches were not included even if they were fished in English waters). That approach relies on the existence of homogeneous trends in landings per unit effort, and data from the UK beam trawl fleet were more suitable than data from the French otter-trawl fleet. UK beam trawlers operate offshore, whereas French trawlers move between inshore and offshore areas, with consequent variations in cuttlefish catchability. The whole English Channel cuttlefish stock was assessed using VPA with a monthly time-scale by Royer et al. (2006). Recruitment strength varied by a factor of two for cohorts in the years 1996–1999. The exploitation pattern suggested greatest fishing mortality at older ages and showed cohorts fully exploited, but without significant growth-overfishing (when catches are made before the cohort reaches maximal biomass). Interactions between fishing fleets underlined the fact that catches of inshore trapfishing depend on the activity of offshore trawlers (which fish the cohorts at a younger stage in winter). It is worth noting that the consequence of trapfishing for adults on recruitment (i.e. recruitment-overfishing) in the trawl fishery could not be estimated in the absence of a stock–recruitment relationship. In small-scale fisheries, like those around the Galician coast, the quality of fishery statistics can be improved using interviews and applying the Gomez–Muñoz model (Rocha et al., 2006). On other fishing grounds, abundance trends have been monitored even if no population model has yet been fitted. Landing-per-unit-effort indices for the Gulf of Cádiz (Sobrino et al., 2002) and for Portuguese waters (Jorge and Sobral, 2004) are useful for analysing fishery and environmental variations. Sepia officinalis fisheries are probably close to their maximum sustainable production in several areas of the species distribution given that negative trends in captures have been observed in recent years in some heavily fished areas (e.g. the Mediterranean). In the European Union, S. officinalis is not a quota species. Nevertheless, some management measures have been implemented at local scales. Minimum landing size restrictions exist in Galicia (8 cm ML) and also in Portugal (Hastie et al., 2009a). The reduction in catches of recruits in France is sought via the progressive banning of trawlers within 3 miles of the coast. Cephalopod biology and fisheries in Europe: II. Species Accounts | 71 Existing fishing effort limitations mainly concern métiers specifically targeting cuttlefish, such as trapfishing. In Normandy (France), the trapfishing fleet is regulated via licences, which also state the number of traps allowed per boat. Common cuttlefish is usually marketed fresh or frozen and is a highly appreciated food item, particularly in European Mediterranean countries, Spain, Portugal, Japan, China, and the Republic of Korea. 6.10 Aquaculture Sepia officinalis adapts easily to laboratory culture because of its large eggs, good survival of hatchlings, voraciousness of the hatchlings, sedentary behaviour, tolerance to crowding and handling, acceptance of dead prey, and easy reproduction in captivity (Forsythe et al., 1994). Therefore, laboratory culture has been successful around the world since the early 1960s (Schröder, 1966; Richard, 1966, 1971, 1975; Pascual, 1978; Yim, 1978; Boletzky, 1979a, 1983; Boletzky and Hanlon, 1983; DeRusha et al., 1989; Lee et al., 1991; Forsythe et al., 1994; Domingues, 1999; Bettencourt, 2000; Domingues et al., 2001b, 2002, 2006). During the first few weeks of their life, cuttlefish have to be fed live prey, usually mysid shrimps (Richard, 1975; Forsythe et al., 1994; Domingues, 1999; Domingues et al., 2001a). Subsequently, they accept dead food such as frozen shrimps, fish, and crabs (De Rusha et al., 1989; Forsythe et al., 1991; Koueta and Boucaud Camou, 1999; Domingues et al., 2001b; Koueta, 2001; Koueta et al., 2002). Some researchers have cultured the species using this transition to dead food (Pascual, 1978; Forsythe et al., 1994), whereas others fed live prey throughout the life cycle (Domingues et al., 2001a, b, 2002). In the past few years, feeding experiments using S. officinalis have been conducted with either moist or dry pellets (Castro, 1990; Lee et al., 1991; Castro et al., 1993) or surimi (fish myofibrillar protein concentrate (Castro et al., 1993; Castro and Lee, 1994; Domingues, 1999; Domingues et al., 2005), demonstrating that cuttlefish readily accept prepared diets. Feeding rates on prepared diets have been considerably lower than with a normal laboratory maintenance diet of crustaceans (Richard, 1971, 1975; Pascual, 1978; Boletzky, 1979a; Lee et al., 1991; Castro et al., 1993; Castro and Lee, 1994; Forsythe et al., 1994; Koueta and Boucaud-Camou, 1999, 2001; Koueta et al., 2000; Domingues et al., 2001b, 2002, 2003a, b, 2004), and also considerably lower than rates during transition periods when cuttlefish were fed thawed catfish fillets. During these transition periods, feeding rate varied between 3.5 and 10% BW d –1 (Domingues, 1999). Despite the acceptance of the prepared diets, negative growth with artificial diets was common, and the fastest growth rates reported in the literature, close to 0.5% BW d –1 (Castro, 1990; Lee et al., 1991; Castro et al., 1993; Castro and Lee, 1994; Domingues, 1999; Domingues et al., 2005) are almost tenfold lower than growth rates recorded during normal laboratory maintenance of this species (5% BW d –1) (Pascual, 1978; Lee et al., 1991; Forsythe et al., 1994; Domingues et al., 2001b, 2002; Sykes et al., 2003). Also, mortality rates when feeding artificial diets are usually higher than with natural diets (DeRusha et al., 1989; Lee et al., 1991; Castro et al., 1993). Effects of polyunsaturated fatty acids (PUFA) in the diet on survival, acceptance of alternative food, and growth of juvenile cuttlefish have been demonstrated (Koueta et al., 2002, 2006). Prey density also affects growth of S. officinalis; faster growth rates were obtained at higher prey density, and vice versa. Because of the ease of culture and progress in culturing methods, S. officinalis is an ideal laboratory animal for various experimental purposes and a useful research model in 72 | ICES Cooperative Research Report No. 325 physiology, neuroscience, nutritional biochemistry, ageing, molecular biology, and immunology (Sykes et al., 2006). 6.11 Future research, needs, and outlook The biology of S. officinalis is relatively well known; it is the most extensively studied of all cuttlefish species. Nevertheless, there are still uncertainties concerning the separation of stocks and populations. The effects of climatic change on the distribution and abundance of S. officinalis populations does need to be studied. Of particular importance is the threat of increasing ocean acidification, because the cuttlebone and statoliths of S. officinalis are calcareous structures, and their development is heavily influenced by pCO2 in seawater. Experimental studies show that during elevated seawater pCO2 conditions, cuttlebone calcification increases (Gutowska et al. 2008, 2010a, b), and that morphology and calcification in statoliths of hatchlings are distorted, leading to abnormalities in balance maintenance and prey-capture efficiency (Maneja et al., 2011). Recent experimental studies demonstrate that diet, temperature, and salinity can affect trace-element composition in the statoliths of S. officinalis (Zumholz, 2005; Zumholz et al., 2006, 2007a). Further, investigations on the carbon- and oxygen- isotope composition and ratios (δ18O, δ13C) of the cuttlebone of S. officinalis have been shown to be a useful a tool for predicting ecological information and environmental history scenarios (e.g. Bettencourt and Guerra, 1999; Rexfort and Mutterlose, 2006). Because of the short life cycle and often dramatic changes in popuation abundance, fishery management of the species is difficult, and stocks require regular monitoring. The current low level of routine fishery data collection on European cephalopods, including S. officinalis, coupled with the high data demands associated with stock assessments, means that analytical assessment is generally impractical. Therefore, the ICES Working Group on Cephalopod Fisheries and Life History recommended examining trends in relative exploitation rates (i.e. catch/survey biomass) by seasonal cohort. The Group also recommended a comparison of maturity and length composition data by cohort, from research surveys and the fishery, in order to assess trends in recruitment and length at 50% maturity (L50) (ICES, 2010). Fundamental to the implementation of any such approach is the collection of reliable species-level landings statistics. To carry out analytical stock assessments on such short-lived species, it is necessary to monitor biological variables regularly, ideally every week or month. Quarterly sampling is insufficient for any cephalopod species. Even length composition sampling should be carried out on a more regular basis in those métiers in which cephalopods are considered as “G2 species”. In order to avoid unnecessary sampling effort, however, sampling should take into account the seasonality of cephalopod landings and discards, with sampling concentrated during times when cephalopod catches are biggest (ICES, 2010). Effective technologies using statoliths and new methods for age determination in this species are also needed. Age determination is important for understanding the demographic structure of populations and hence to improve the sustainable exploitation of this species. Finally, study of anthropogenic contaminant bioaccumulation would improve knowledge of the effects of these toxins on the recruitment phase and on the quality of mature animals as human food. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Sepia elegans Elegant cuttlefish | 73 74 | 7 ICES Cooperative Research Report No. 325 Sepia elegans Blainville, 1827 Patrizia Jereb, Ignacio Sobrino, A. Louise Allcock, Sonia Seixas, and Evgenia Lefkaditou Common names Seiche élégante (France), seppia elegante (Italy), choco-elegante (Portugal), choquito (Spain), elegant cuttlefish (UK) (Figure 7.1). Synonyms Sepia rupellaria Férussac and d’Orbigny, 1835, Sepia biserialis Blainville, 1827, Sepia italica Risso, 1854. 7.1 Geographic distribution The elegant cuttlefish, Sepia elegans Blainville, 1827, is found in the Northeast Atlantic, from northwestern Scotland and Ireland (Massy, 1928; Stephen, 1944; Nesis, 1982/87) (Figure 7.2) down to Namibia (Sánchez, 1988; Roeleveld, 1998). It is present in the Celtic Sea (Lordan et al., 2001a) and the English Channel (Marine Biological Association of the United Kingdom, 1931; Roper and Figure 7.1. Sepia elegans. Dorsal view. Sweeney, 1981) and off the French and IbeFrom Guerra (1992) rian Atlantic coasts (Guerra, 1992). It is caught on the Sahara Bank (e.g. Bravo de Laguna, 1989; Balguerias et al., 2000) and extends south to northern Namibian waters (Sánchez, 1988), where it has been recorded at 21°S (Roeleveld, 1998). Records from the Agulhas Bank exist (Filippova et al., 1995), but, as noted by Roeleveld (1998), the geographic position reported by the authors is apparently incorrect. Sepia elegans is also widely distributed throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello 2004; Salman, 2009), including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak et al., 2008). It has been recorded in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Cephalopod biology and fisheries in Europe: II. Species Accounts | 75 Figure 7.2. Sepia elegans. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 7.2 Taxonomy 7.2.1 Systematics Coleoidea – Decapodiformes – Sepiida – Sepiidae – Sepia. 7.2.2 Type locality Sicily, central Mediterranean Sea. 7.2.3 Type repository Originally Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. Syntypes; specimens not extant [fide Lu et al. (1995:315)]. 7.3 Diagnosis 7.3.1 Paralarvae This species does not have paralarvae sensu Young and Harman (1988). Hatching size is assumed to be 4 mm ML (Mangold-Wirz, 1963a). 7.3.2 Juveniles and adults Sepia elegans is a small species, with adult males growing up to 75 mm ML (Ciavaglia and Manfredi, 2009) and females up to 89 mm ML (Adam, 1952). Maximum total weight is ca. 60 g. The mantle is oblong, more than twice as long as wide, with the dorsal anterior margin triangular, acute, and projecting strongly forward. Male and female arms are subequal in length. The left ventral arm is hectocotylized in males (Figure 7.3). It bears 1–2 rows of normal-sized suckers proximally, followed by 9–11 76 | ICES Cooperative Research Report No. 325 rows of reduced minute suckers medially, followed by normal-sized suckers to the arm tip; suckers are set in two dorsal and two ventral series displaced laterally. Figure 7.3. Sepia elegans. Left arm III hectocotylized. Photo: Carlos Farias. Tentacular clubs are short and oval, and the sucker-bearing surface is flattened. There are 6–8 suckers in transverse rows. Suckers differ markedly in size. There are 3–4 greatly enlarged suckers in the middle of the club, and although several dorsal suckers are enlarged, they are never as large as the medial suckers. The cuttlebone is oblong and convex in lateral view. It tapers to a sharp point anteriorly and posteriorly, is recurved ventrally, and its dorsal surface is evenly convex. The last loculus is convex. The anterior striae are an inverted U-shape. The spine is very small, “rather like a small calcareous ridge than a true spine” (Nesis, 1982/1987). Lateral wings are present, but are very small. The animal is reddish brown in life, but paler than S. orbignyana. There are a few scattered chromatophores on the head, and the dorsal mantle surface is peppered with scattered purple-black chromatophores, but the fins and the ventral mantle surface are pale (Adam and Rees, 1966; Nesis, 1982/1987; Neige and Boletzky, 1997; Reid et al., 2005). The beaks are illustrated in Figure 7.4. Figure 7.4. Sepia elegans. Lower beak (left) and upper beak (right). Photo: Carlos Farias. Cephalopod biology and fisheries in Europe: II. Species Accounts 7.4 | 77 Remarks Floating cuttlebones may enter the eastern side of the North Sea and be found stranded on the Belgian and Dutch coasts (Adam, 1933); however, live S. elegans have never been found in the North Sea (e.g. Adam, 1933; Roper and Sweeney, 1981; Nesis, 1982/87). Recent observations confirm this (J. Goud, pers. comm.). The species has been reported from the Agulhas Bank (37°12’S 22°30’E) by Filippova et al. (1995), but as noted by Roeleveld (1998), the position given in Filippova’s paper is incorrect because it lies south of the Agulhas Bank, in ca. 4000 m depth. On the basis of morphological features (Khromov, 1987a; Khromov et al., 1998), and, subsequently, genetic divergence (Pérez-Losada et al., 1996; Sanjuan et al., 1996), it has been suggested that S. elegans and S. orbignyana belong to a different subgenus from the genus Sepia sensu stricto, i.e. to the subgenus Rhombosepion. Morphometric analysis of both cuttlebone and statoliths, based on landmarks, may prove a useful taxonomic tool for the separation of S. elegans from closely related species (Neige and Boletzky, 1997; Lombarte et al., 2006). 7.5 Life history Although this species spawns year-round, seasonal migrations and seasonal peaks in spawning have been described in some areas. It lives for 12–18 months. There is no paralarval stage. 7.5.1 Egg and juvenile development The eggs (maximum recorded diameter 5 mm; Guerra, 1984) are attached to available hard substrata, such as alcyonarian (typically Alcyonium palmatum) shells, on muddy bottoms, or, less frequently, on coral formations (Mangold-Wirz, 1963a). They closely resemble S. officinalis eggs, except for the dimensions (smaller in S. elegans) and colour (whitish and translucent in S. elegans). The attachment of the eggs to Alcyonium palmatum is quite an elaborate and complex procedure, at the end of which the egg resembles a stone on a ring slipped onto the alcyonarian finger-like appendage, as described in detail by Bouligand (1961). After hatching, juveniles immediately adopt a benthic lifestyle. 7.5.2 Growth and lifespan Growth in mantle length is 2.8 mm month–1 for males and 3.0 mm for females in the Sicilian Channel (central Mediterranean) (Ragonese and Jereb, 1991), i.e. slightly faster than estimated in the western Mediterranean by Mangold-Wirz (1963a) and in the Ría de Vigo by Guerra (1984) (2–2.5 mm month–1). Females attain larger size and are comparatively heavier than males at any given mantle length, and animals become more slender as size increases (Bello, 1988; Guerra and Castro, 1989; Ragonese and Jereb, 1991; Lefkaditou et al., 2007; Ramos et al., 2009; A. Moreno, unpublished data). The largest individuals recorded by Guerra and Castro (1989) were 61 mm ML (males) and 67 mm ML (females). Length–weight relationships are available for several areas (Table 7.1). Female tentacular clubs are significantly longer than male ones (Bello, 1991a). Bello and Piscitelli (2000) showed that S. elegans females ingest more food at any given size and suggested that a cause–effect relationship between sex-related club size and growth rate existed. Subsequent observations on S. elegans and S. orbignyana demonstrated the existence of a positive correlation between body condition and tentacular club length in males and females of both species (Bello, 2006), and strongly corroborated the hypothesis that there is indeed a cause–effect relationship. 78 | ICES Cooperative Research Report No. 325 From observations in the field, lifespan is estimated to range between 12 and 18–19 months (Mangold-Wirz, 1963a; Guerra, 1984; Guerra and Castro, 1989), somewhat less than the values obtained by preliminary estimates with length-frequency distribution analysis (i.e. ca. 2 years, Ragonese and Jereb, 1991). However, length-frequency distributions are generally polymodal (see also Guerra and Castro, 1989), making it difficult to identify microcohorts clearly, and growth estimation by means of length-frequency methods is difficult (e.g. Caddy, 1991). Table 7.1. Sepia elegans. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Ría de Vigo 0.374 2.272 F Guerra and Castro (1989) 0.327 2.311 M 0.289 2.420 F 0.356 2.190 M 0.239 2.476 F 0.227 2.577 M 0.257 2.506 F 0.286 2.342 M 0.196 2.606 F 0.208 2.500 M 0.229 2.515 F 0.248 2.441 M Portuguese waters Gulf of Cádiz Sicilian Channel Adriatic Sea Aegean Sea 7.5.3 A. Moreno, pers. comm. Ramos et al. (2009) Ragonese and Jereb (1991) Bello (1988) Lefkaditou et al. (2007) Maturation and reproduction In the Ría de Vigo, males outnumber females in spring and autumn, and the overall sex ratio recorded by Guerra and Castro (1989) was 1.18:1 in favour of males. The smallest mature males measure 20 mm ML (Volpi et al., 1990), and the smallest mature females 30 mm ML (Guerra and Castro, 1989). In Portuguese waters, ca. 60– 70% of males and females are mature at ca. 35 and 45 mm ML, respectively (A. Moreno, pers. comm.), and in the Catalan Sea (western Mediterranean), the equivalent figures are 45 mm ML for males and 65 mm ML for females (Mangold-Wirz, 1963a). In the Mediterranean and the eastern Atlantic, mature males and females are found throughout the year, which suggests a continuous spawning period (Mangold-Wirz, 1963a; Guerra, 1992; Belcari, 1999a; Reid et al., 2005). As a consequence of this, recruitment is virtually continuous, although alternating peaks and troughs have been observed in the Mediterranean (Bello, 1983–1984; Casali et al., 1988; Volpi et al., 1990; Jereb and Ragonese, 1991a; Würtz et al., 1991; D’Onghia et al., 1992; Ciavaglia and Manfredi, 2009), and two major peaks, one in spring–summer the other in late autumn–mid-winter, have been observed in the Gulf of Cádiz (eastern Atlantic; Ramos et al., 2009). In the Catalan Sea, spermatophore length ranges between 3.5 and 5.5 mm, depending on male size, and the maximum number of spermatophores found in a mature male has been 95. Mature, smooth eggs measure between 3.7 and 4.2 mm, depending on female size, and mature females carry up to 250 eggs (>1 mm) in their ovaries; however, as is normal for “large” eggs in cephalopods, only a proportion of the eggs reach maturity (Mangold-Wirz, 1963a). It is difficult to establish a correlation between the total Cephalopod biology and fisheries in Europe: II. Species Accounts | 79 number of smooth eggs in the ovary and the actual total number of smooth eggs produced by a female, because spawning is protracted; when captured, mature females may already have spawned a fraction of their smooth eggs. The maximum number of smooth eggs recorded in a mature female (of 62 mm ML) was 57 (Mangold-Wirz, 1963a). Total fecundity in females from the Gulf of Cádiz varied between 61 and 942 oocytes (in specimens of 34 and 64.2 mm ML, respectively). 7.6 Biological distribution 7.6.1 Habitat Sepia elegans is a sublittoral species, living on sandy and sand-muddy bottoms. It has been found at various depths, from very shallow (e.g. 2 m in the Ría de Vigo, northwestern Spain, Guerra, 1985a; 6 m in the northern Tyrrhenia Sea, Belcari and Sartor, 1993; 12 m in the southern Tyrrhenian Sea, Bello et al., 1994) down to 494 m (Jereb and Ragonese, 1991a). Records deeper than 450 m are sporadic (e.g. Jereb and Ragonese, 1991a; D’Onghia et al., 1996; Lefkaditou et al., 2003a; A. Moreno, pers. comm.), and most distributional ranges reported for the Mediterranean and the eastern Atlantic indicate maximum depths of <400 m (Adam, 1952; Mangold-Wirz, 1963a; Lumare, 1970; Guerra, 1985a, Sánchez, 1986a; Mannini and Volpi, 1989; Katağan and Kokatas, 1990; Würtz et al., 1991; D’Onghia et al., 1992; Belcari and Sartor, 1993; Bello et al., 1994; González and Sánchez, 2002; Relini et al., 2002; Massutí and Reñones, 2005). It is the peculiar structure of the cuttlebone, which is small, narrow, with closely packed septa, and modified sutures (Ward, 1991), that allows S. elegans to reach these remarkable depths and to be among the deepest living Sepia species known. However, depths below the maximum recorded may be lethal for the species (Ward and Boletzky, 1984). The depth ranges at which maximum concentrations of animals are found vary between areas and seasons (Mangold-Wirz, 1963a; Sánchez, 1986a; Restuccia and Ragonese, 1986; Jereb and Ragonese, 1991a; Würtz et al., 1991; Sánchez et al., 1998a; Belcari, 1999a; Colloca et al., 2003). In addition, migrations can be related to reproduction (see below). In the Sea of Marmara, the species has been found in brackish waters (salinity between 18 and 25; Ünsal et al., 1999), but in northwestern Spain, it inhabits the outer and central basin of the Ría de Vigo (Guerra 1985a; Guerra and Castro, 1989), indicating a high degree of tolerance to salinity variation, although the species does not enter the internal basin of the Ría de Vigo, where there are marked fluctuations in salinity and temperature (Guerra and Castro, 1989). This indicates that S. elegans is a more stenohaline and stenothermic species than S. officinalis. 7.6.2 Migrations A spring–summer migration of the whole population to coastal spawning grounds (40– 70 m depth) has been described for the species in the western Mediterranean (Mangold-Wirz, 1963a; Guerra, 1992), and similar displacements have been observed in the Tyrrhenian Sea (off the Tuscany coast; Belcari, 1999a). However, this migratory pattern does not seem to be displayed in other areas, such as the Ría de Vigo (northwestern Spain; Guerra and Castro, 1989) or the Sicilian Channel (Jereb and Ragonese, 1991a), and both presence and absence of migration have been reported for the Adriatic Sea (Casali et al., 1988; Ciavaglia and Manfredi, 2009). 80 | 7.7 ICES Cooperative Research Report No. 325 Trophic ecology 7.7.1 Prey The species feeds mainly on small crustaceans, fish, and polychaetes (Reid et al., 2005) (Table 7.2). Detailed studies on feeding (e.g. Guerra, 1985b; Castro and Guerra, 1990) suggested that neither diet composition nor prey size varied with body size or maturity. No seasonal changes in diet were observed. However, Bello (1991a, 2006) reported differences in feeding habits between males and females; females eat significantly larger quantities of crabs (Brachyura) and shrimps (Palaemonidae) than males, and the average weight of the stomach contents is greater in females. In the Thermaikos Gulf, Greece, the species feeds mainly on crustaceans and secondarily on fish, and the trophic level is estimated to be 3.53 (Fryganiotis et al., 2007). Table 7.2. Prey composition of Sepia elegans, as known from studies in the Northeast Atlantic and the eastern Mediterranean Sea (compiled from Guerra, 1985b1; Castro and Guerra, 19902; Vafidis et al., 20093). Taxon Species Osteichthyes Callionymidae Callionymus lyra (dragonet)2, Gobiidae Aphia minuta (transparent goby)1, indet.2, Pomatoschistus pictus (painted goby)2 Crustacea Decapoda Pleocyemata- Galathea intermedia2, Porcellana platycheles2, Pisidia longicornis1,2 Anomura Pleocyemata- Liocarcinus spp.1,2, Polybius henslowii1, Portunidae indet.2, indet.3 Brachyura Pleocyemata- Crangon crangon1,2, Hippolytidae indet.2, Majidae indet.2, Palaemon Caridea adspersus1,2, P. serratus1, Palaemon spp.2, Palaemonidae indet.2, Processa edulis2, indet.3 Euphausiacea indet.3 Mysida indet.2 Ostracoda indet.3 Amphipoda Caprellidea indet.2, Gammarus spp.1, Gammaridea indet.2, indet.3 Isopoda indet.3 Cephalopoda indet.3 Polychaeta indet.2,3 Nemertea indet.3 Cnidaria Hydrozoa indet.3 Algae Posidonia oceanica1, Zostera marina1, indet.1 7.7.2 Predators Sepia elegans has been found in the stomachs of several fish species, including mediumsized hake (Merluccius merluccius) (18–44 cm) in the Gulf of Cádiz (Á. Torres, pers. comm.). It is also preyed upon by S. officinalis and Loligo vulgaris off the south coast of Portugal (Coelho et al., 1997; Alves et al., 2006) and is eaten by the bottlenose dolphin (Tursiops truncatus) in Spanish waters of the western Mediterranean Sea (Blanco et al., 2001) (Table 7.3). Cephalopod biology and fisheries in Europe: II. Species Accounts | 81 Table 7.3. Known predators of Sepia elegans in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalop- Common cuttlefish (Sepia officinalis) Alves et al. (2006) European squid (Loligo vulgaris) Coelho et al. (1997) Chondrich- Lesser spotted dogfish (Scyliorhinus ca- Kabasakal (2002), Šantić et al. thyes nicula) (2012) Bull ray (Pteromylaeus bovinus) Capapé (1977) Marbled electric ray (Torpedo mar- Capapé et al. (2007) oda morata) Thornback ray (Raja clavata) Kabasakal (2002), Šantić et al. (2012) Osteich- Common dolphinfish (Coryphaena hip- thyes purus) Cetacea 7.8 Massutí et al. (1998) European hake (Merluccius merluccius) Á. Torres, pers. comm. Greater amberjack (Seriola dumerili) Matallanas et al. (1995) John Dory (Zeus faber) Silva (1999b) Bottlenose dolphin (Tursiops truncatus) Blanco et al. (2001) Other ecological aspects 7.8.1 Parasites Females harbour a dense bacterial community in their accessory nidamental glands, in the lumina of these organs’ tubules (Grigioni et al., 2002), as observed in other sepiolids and myopsid squids. Information on the effects of this bacterial community on S. elegans physiology is lacking, although studies on bacterial presence in S. officinalis revealed correlations between sexual maturity, the colour of the gland, and the total number of bacteria (Van den Branden et al., 1980). Parasites of S. elegans include Aggregata sp. and Pennella sp. (González et al., 2003). 7.8.2 Contaminants High levels of cadmium have been reported in the elegant cuttlefish (Bustamante et al., 2002b), indicating that efficient detoxification mechanisms have been developed. The high bioavailability of cadmium in the digestive gland cells also indicates a high potential for the trophic transfer of the metal to predators of S. elegans. Studies on biochemical composition of tissues distinguished this species from others with a benthic lifestyle and indicated lower lipid and higher protein contents in the gonad (Rosa et al., 2005a). 7.9 Fisheries Sepia elegans is one of the most abundant cephalopod species in the Catalan Sea, Tyrrhenian Sea, Sicilian Channel, Adriatic Sea, Ionian Sea, and Aegean Sea (MangoldWirz, 1963a; Lumare, 1970; Mandić and Stjepcević, 1983; Panetta et al., 1986; Sánchez, 1986a; Jereb and Ragonese, 1991a; Würtz et al., 1991; Belcari and Sartor, 1993; D’Onghia et al., 1996). It is taken mainly as bycatch in the Mediterranean and West African bottom otter-trawl fisheries. Other fishing gears that catch the species include beam trawls (Ünsal et al., 1999) and fish traps (Belluscio and Ardizzone, 1990), and S. elegans represents a major fraction of discards in southern Portuguese coastal fisheries (Sendao et al., 2002). 82 | ICES Cooperative Research Report No. 325 Separate landing statistics are not reported for this species, which, however, represents a significant percentage of the catches in some areas of its distributional range, where it is marketed fresh and frozen (Reid et al., 2005). In the Mediterranean, it is marketed along with S. orbignyana and small S. officinalis and constitutes a valuable resource locally (Jereb and Ragonese, 1991a). In the Sicilian Channel, research estimated an exploitation rate of 0.73 for the species, which suggests intense fishing pressure on the resource (Ragonese and Jereb, 1991). In the Gulf of Cádiz in the eastern Atlantic, landings ranged between 30 and 110 t year–1 in the period 1993–2008 (I. Sobrino, pers. comm.). 7.10 Future research, needs, and outlook Of the three genera currently recognized within the family Sepiidae (see Khromov et al., 1998, for a recent review), Sepia is the most speciose; more than 100 species have been described. However, many species are poorly known, and the systematics of the genus is not yet settled. Among the many questions still unresolved is the validity of the subdivision of the genus into six subgenera or “species complexes” (see Khromov et al., 1998; see also the Remarks section). Further research is needed to clarify the systematics of the group and the position of this species within the group. The species is an important resource in many areas of its distributional range and is subjected to intense fishing pressure in some areas. Detailed studies on its ecology might help preclude potential overexploitation, and separate recording of different cuttlefish species in landings should be encouraged. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Sepia orbignyana Pink cuttlefish | 83 84 | 8 ICES Cooperative Research Report No. 325 Sepia orbignyana Férussac in d’Orbigny, 1826 Patrizia Jereb, Ignacio Sobrino, A. Louise Allcock, Sonia Seixas, and Evgenia Lefkaditou Common names Seiche rosée (France), Κοκκινοσουπιά [kokkinosoupia] (Greece), seppia pizzuta (Italy), choco-de-cauda (Portugal), choquito picudo (Spain), pink cuttlefish (UK) (Figure 8.1). Synonyms Acanthosepion orbignyanum Rochebrune, 1884, Sepia rubens Philippi, 1844, Acanthosepion enoplon Rochebrune, 1884. 8.1 Geographic distribution The pink cuttlefish, Sepia orbignyana Férussac in d’Orbigny, 1826, is found in the Northeast Atlantic and throughout the Mediterranean (Nesis, 1982/1987; Roper et al., 1984; Guerra, 1992; Reid and Jereb, 2005) (Figure 8.2), although the northern limits of its distribution are unclear. It is reported in the Irish Sea and the English Channel (Nesis, 1982/87, Reid and Jereb, 2005), but it is not Figure 8.1. Sepia orbignyana. Dorsal view. included among the species listed by Massy From Guerra (1992). (1928) for the Irish coast. In addition, although Adam (1952) indicates that its distribution extends to the Arcachon Basin (western France), there is no mention of its presence along the east coast of England in old records (e.g. Grimpe, 1925), and the reference to the English Channel by Norman (1890, p. 484 in Stephen, 1944) apparently is a misquotation. Strandings of cuttlebones of this species are, however, known from North Sea coasts (e.g. the Netherlands; Cadee, 2002). The species can be found south along the French and Spanish coasts (Morales, 1958; Adam and Rees, 1966), in the Bay of Biscay, south to ca. 17°S (southern Angola; Adam, 1962). Sepia orbignyana is widely distributed throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009) including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a, Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea, although it is only rarely caught in the northern part (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997; 1998; Lefkaditou et al., 2003b). The species has been recorded also in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Cephalopod biology and fisheries in Europe: II. Species Accounts | 85 Figure. 8.2. Sepia orbignyana. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 8.2 Taxonomy 8.2.1 Systematics Coleoidea – Decapodiformes – Sepiida – Sepiidae – Sepia. 8.2.2 Type locality La Rochelle, France. 8.2.3 Type repository Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. [fide Lu et al. (1995: 322)]. 8.3 Diagnosis 8.3.1 Paralarvae This species does not have paralarvae sensu Young and Harman (1988). Animals newly hatched in the laboratory measure ca. 6 mm ML (Boletzky, 1988). 8.3.2 Juveniles and adults Sepia orbignyana is a small species, with adult males up to 96 mm and females up to 120 mm ML (Mangold-Wirz, 1963a). The mantle is oval, with the dorsal anterior margin projecting strongly (Figure 8.3). Male and female arms are subequal in length and rather short. Arm suckers are tetraserial. Medial suckers on the non-hectocotylized arms of males are wider than marginal suckers. The left ventral arm is hectocotylized in males: 1–2 rows of normal size suckers are present proximally, followed by greatly reduced suckers medially, then normal size suckers at the distal end to the arm tip. 86 | ICES Cooperative Research Report No. 325 Suckers of the hectocotylus are arranged in two dorsal and two ventral series displaced laterally. Clubs are short, oval, and bear 5–6 suckers in transverse rows; suckers vary markedly in size. Three large suckers are present medially with one slightly smaller sucker on each side of them. The cuttlebone is oblong, acute anteriorly, bluntly rounded posteriorly, and strongly recurved ventrally; its dorsal surface is rose-coloured or orange. Shell width is ca. 33% and 33–35% of shell length in males and females, respectively. The spine is long, pointed, and straight, directed slightly upwards, with a ventral keel. The anterior striae are shallow, M-shaped, or wavy. The animal’s colour is reddish brown. (Adam and Rees, 1966; Nesis, 1982/1987; Neige and Boletzky, 1997; Reid et al., 2005). Figure 8.3. Sepia orbignyana. Dorsal view. Photo: IAMC-CNR (Mazara del Vallo, Sicily, Mediterranean Sea) research team. 8.4 Remarks Floating cuttlebones may enter the southeastern North Sea and be found stranded on the Belgian coast (Eneman and Kerckhof, 1983; Nesis, 1982/1987). However, although Muus (1963) mentioned the presence of the species in the southern North Sea, no other records of live S. orbignyana from these waters exist (e.g. Adam, 1933; Adam and Rees, 1966; Nesis, 1982/1987), as confirmed also by very recent studies (J. Goud, pers. comm.). On the basis of the animal’s morphology (Khromov, 1987a; Khromov et al., 1998), and, subsequently, results on genetic divergence (Pérez-Losada et al., 1996; Sanjuan et al., 1996), it has been suggested that S. orbignyana and S. elegans belong to the subgenus Rhombosepion within the genus Sepia. Morphometric analysis of cuttlebone and statolith shape based on landmarks may prove a useful taxonomic tool to distinguish S. orbignyana from closely related species (Neige and Boletzky, 1997; Lombarte et al., 2006). 8.5 Life history Lifespan is 12–18 months. Spawning shows a clear summer peak in the Atlantic, but is year-round in the Mediterranean. As with other members of the genus, the hatchlings immediately adopt a benthic life style. Cephalopod biology and fisheries in Europe: II. Species Accounts 8.5.1 | 87 Egg and juvenile development Eggs are laid in batches of 30–40 and are individually introduced into the tissues of sponges, usually Demospongiae, on muddy bottoms (Boletzky, 1998). The sponge provides protection for the eggs. The eggs are whitish-grey in colour, and their gelatinous envelop is less thick than that of other studied species (features which probably represent an adaptation to the “host organism” used to protect the eggs), although the chorion is very hard (Mangold-Wirz, 1963a). Egg diameter increases with the size of the females; maximum reported egg size is 9 mm (Mangold-Wirz, 1963a). Information on S. orbignyana juveniles comes from rearing experiments (Boletzky, 1988). Newly hatched animals measure ca. 6 mm ML. They immediately settle on the substratum and move only over short distances by active swimming as well as by slowly “walking” along the bottom on their ventral arms. They have not been seen to bury themselves in soft substratum, as typical for S. officinalis, but they vigorously raise their dorsal arms and quickly wave them laterally when disturbed. They are able to adhere very efficiently to hard substrata by the ventral skin. 8.5.2 Growth and lifespan In the Catalan Sea, growth rates of females have been reported to be slightly faster than those of males (Mangold-Wirz, 1963a). Studies of populations in the Sicilian Channel (central Mediterranean) by Ragonese and Jereb (1991) confirmed this finding and reported growth rates of 2.9 mm month–1 in males and 3 mm in females. Additional support for these results has subsequently come from studies in the Adriatic Sea (Bello, 1988, 2001), Aegean Sea (Lefkaditou et al., 2007), and Portuguese waters. Bello (2001) used the number of chambers in the cuttlebone as an index of relative age. Females also attain significantly larger size than males and are notably heavier (Bello, 1988; Ragonese and Jereb, 1991). Length–weight relationships are summarized in Table 8.1. All studies reported “b” exponent values <3 in both sexes, showing that animals become more slender as size increases. Table 8.1. Sepia orbignyana. Length–weight relationships in different geographic areas for females (F) and males (M). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Portuguese waters 0.337 2.486 F A. Moreno, pers. comm. 0.284 2.340 M 0.6567 2.15 F 0.4052 2.35 M 0.266 2.58 F 0.272 2.480 M 0.224 2.560 F 0.208 2.558 M 0.343 2.305 F 0.525 2.441 M Catalan Sea Sicilian Channel Adriatic Sea Aegean Sea Sánchez (1986) Ragonese and Jereb (1991) Bello (1988) Lefkaditou et al. (2007) Female tentacular clubs are significantly longer than male ones (Bello, 1991a). Subsequently, Bello and Piscitelli (2000) showed that S. orbignyana females ingest more food at any given size and suggested a cause–effect relationship between sex-related club size and growth rate. Additional observations on S. orbignyana and S. elegans demonstrated the existence of a positive correlation between body condition and tentacle club 88 | ICES Cooperative Research Report No. 325 length in males and females of both species (Bello, 2006) and strongly corroborated the hypothesis that there is indeed a cause–effect relationship. Lifespan is estimated to be 12–18 months (Mangold-Wirz, 1963a), although preliminary estimates from analysis of length-frequency distributions suggested a longer life, i.e. ca. 3 years (Ragonese and Jereb, 1991). As in many cephalopods, length-frequency distributions generally are polymodal, although it is difficult to identify microcohorts, and growth estimation by means of length-frequency methods is generally unreliable for cephalopods (e.g. Caddy, 1991). 8.5.3 Maturation and reproduction A predominance of females in June–July is reported for the species in Portuguese waters (A. Moreno, pers. comm.). In the Mediterranean, the smallest recorded mature male measured 35 mm ML (Belcari and Sartor, 1993), and the smallest mature female, a recent record from the Adriatic Sea, measured 40 mm ML (Ciavaglia and Manfredi, 2009). In Portuguese waters, slightly smaller sizes at first maturity have been observed, i.e. 29 mm ML for males and 32 mm ML for females (A. Moreno, pers. comm.). In the Catalan Sea, ca. 60% of males and females are mature at 50 mm and 80 mm ML, respectively (Mangold-Wirz, 1963a). Equivalent figures for Portuguese waters are 47 mm ML for males and 65 mm ML for females (A. Moreno, pers. comm.). In Mediterranean waters, spawning is probably year-round (Mangold-Wirz, 1963a; Jereb and Ragonese, 1991a; Belcari and Sartor, 1993; Ciavaglia and Manfredi, 2009), with peaks of activity from spring to autumn. Recruitment also appears to be continuous throughout the year, with peaks in spring and autumn (Jereb and Ragonese, 1991a; Würtz et al., 1991). Spermatophore length ranges between 5 and 11 mm, and mature males can carry up to 100–150 spermatophores. Mature, smooth, eggs measure 7–9 mm, depending on female size, and mature females may carry up to 400 eggs (>1 mm) in their ovaries; however, as is usually the case for “large” eggs in cephalopods, probably only a fraction reaches maturity (Mangold-Wirz,1963a). It is possible that mature females have already spawned a proportion of their smooth eggs when examined, so the number of smooth eggs in the ovary is not representative of the total number of smooth eggs produced by the female. The maximum number of smooth eggs recorded in a mature female of 91 mm ML was 113 (Mangold-Wirz, 1963a). 8.6 Biological distribution 8.6.1 Habitat The depth range reported for S. orbignyana extends from very shallow (15–20 m; Belcari and Sartor, 1993; Bello et al., 1994; Casali et al., 1998; Ciavaglia and Manfredi, 2009; I. Sobrino, pers. comm.) down to maximum recorded depths of 565 m in the Mediterranean Sea (Cuccu et al., 2003a) and 580 m in the eastern Atlantic (Gulf of Cádiz, I. Sobrino, pers. comm.). However, the species is most abundant between 50 and 250 m throughout the Mediterranean Sea, as confirmed by numerous studies (Mangold-Wirz, 1963a; Adam, 1952; Lumare, 1970; Restuccia and Ragonese, 1986; Sánchez, 1986a; Auteri et al., 1988; Mannini and Volpi; 1989; Soro and Piccinetti-Manfrin, 1989; Katağan and Kocatas, 1990; Repetto et al., 1990; Jereb and Ragonese, 1991a; Würtz et al., 1991; D’Onghia et al., 1992; Belcari and Sartor, 1993; Katağan et al., 1993; Salman et al., 1997; Quetglas et al., 2000; González and Sánchez, 2002; Ciavaglia and Manfredi, 2009). There Cephalopod biology and fisheries in Europe: II. Species Accounts | 89 is also a major concentration of the species between 340 and 360 m in the Gulf of Cádiz (eastern Atlantic, I. Sobrino, pers. comm.). As in S. elegans, it is the peculiar structure of the cuttlebone, which is small, narrow, and with closely packed septa and modified sutures (Ward, 1991), that allows this species to reach these remarkable depths and to be among the deepest living Sepia species known. Records from below 450 m are scarce (e.g. Lefkaditou et al., 2003a), and captures below 550 m extremely so, because that is the depth below which the shell starts to implode (Ward and Boletzky, 1984). The pink cuttlefish is a demersal species that lives mainly on sandy and sandy-muddy bottoms. It is frequently sympatric (and confused) with S. elegans (e.g. Jereb and Ragonese, 1991a), and has been found associated with the horned octopus (Eledone cirrhosa) in some areas (Lumare, 1970). In the Sea of Marmara, the species can live in brackish waters (Ünsal et al., 1999), and in Portuguese waters, it prefers water temperatures >12°C (A. Moreno, pers. comm.). Studies on the demersal assemblages in the Moroccan southern Atlantic zone (Serghini et al., 2008) indicate that the distribution of S. orbignyana is characterized by marked spatial and temporal variability. 8.6.2 Migrations In the Mediterranean, males and females are usually found together throughout the year, and no onshore spawning migrations have been reported (Mangold-Wirz, 1963a; Jereb and Ragonese, 1991a; D’Onghia et al., 1992; Ciavaglia and Manfredi, 2009). 8.7 Trophic ecology 8.7.1 Prey Sepia orbignyana feeds mainly on crustaceans, but small fish, cephalopods, and other invertebrates can also form part of the diet (Table 8.2). In captivity, it will feed on small prawns and mysids (Boletzky, 1988). Table 8.2. Prey composition of Sepia orbignyana, as known from studies in the eastern Atlantic and the Mediterranean Sea (compiled from Allué et al. 19771; Auteri et al., 19882; Vafidis et al., 20093). Taxon Order / Species Osteich- indet.1,2,3 thyes Crustacea Decapoda-Natantia indet.3, Decapoda-Brachyura indet.3, Mysida indet.3, Amphipoda indet.3, Tanaidacea indet.3, indet.1,2 Mollusca Cephalopoda indet.1,2,3, indet.1 Poly- indet.3 chaeta Echinodermata Crinoi- Leptometra phalangium2 dea Ophiuroidea Ophiothrix quinquemaculata2 90 | ICES Cooperative Research Report No. 325 8.7.2 Predators Very little information is available as to which species prey on S. orbignyana, but it has been found in the stomachs of at least three fish species (Table 8.3). In some cases, however, its presence in the stomach contents of scavenger species, such as the lesser spotted dogfish (Scyliorhinus canicula) (Olaso et al., 2002) or seabirds, such as Audouin’s gull (Larus audouinii) (Oro et al., 2008), is most probably attributable to its being discarded by fisheries. Scars found on cuttlebones have been interpreted as toothmarks (Bello and Paparella, 2003). Table 8.3. Known predators of Sepia orbignyana in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Chondrich- Lesser spotted dogfish (Scyliorhinus canicula) I. Sobrino, pers. comm. Thornback ray (Raja clavata) Kabasakal (2002) Osteichthyes Black-bellied anglerfish (Lophius budegassa) I. Sobrino, pers. comm. Aves Audouin’s gull (Larus audouinii) Oro et al. (2008) thyes 8.8 Other ecological aspects 8.8.1 Contaminants High levels of cadmium have been reported in the pink cuttlefish (Bustamante et al., 2002b), indicating that it has efficient detoxification mechanisms. The high bioavailability of cadmium in the digestive gland cells also indicates a high potential for the trophic transfer of this metal to its predators. 8.8.2 Biochemistry Studies on the biochemical composition of tissues indicate a lower lipid content and higher protein content in the gonad than in other cephalopod species with a benthic lifestyle (Rosa et al., 2005a). 8.9 Fisheries Sepia orbignyana is one of the most abundant cephalopod species in some areas of the Mediterranean, i.e. Catalan Sea, Tyrrhenian Sea, Sicilian Channel, southern Adriatic Sea, and Aegean Sea (Mangold-Wirz, 1963a; Lumare, 1970; Mandić and Stjepcević, 1983; Sánchez, 1986a; Jereb and Ragonese, 1991a; Würtz et al., 1991; D’Onghia et al., 1992, 1996; Belcari and Sartor, 1993). It is taken mainly as bycatch, both in the Mediterranean and in West African otter-trawl fisheries. Separate landing statistics are not reported, but S. orbignyana represents a significant percentage of the catches in some areas. In the Mediterranean Sea, it is marketed fresh and frozen, along with S. elegans and small S. officinalis, and constitutes a valuable resource locally. In the Sicilian Channel, research studies have shown an exploitation rate of 0.60 for this species, which suggests intense fishing pressure (Ragonese and Jereb, 1991). More recent studies on the selectivity of diamond, hexagonal, and square-mesh codends (Tosunoğlu et al., 2009) confirmed that the current legal minimum mesh size and codend configurations for demersal trawling are not suitable for regulating fishing on this species, or indeed on other cephalopod species. Cephalopod biology and fisheries in Europe: II. Species Accounts 8.10 | 91 Future research, needs, and outlook Sepia is the most speciose genus of the Sepiidae, but many species are poorly known, and the systematics of the genus are not clearly resolved (see Khromov et al., 1998, and Reid et al., 2005, for recent reviews). Khromov et al. (1998) proposed subdivision of the genus into six “species complexes”, but genetic data are still required to test this idea. Further research is needed to clarify the systematics of the group and the position of this species within the group. Considering the relative importance of the resource in many areas of its distributional range and the intense fishing pressure detected in some of these areas, detailed studies on ecological aspects would be welcome to avoid potential overexploitation. It is essential that separate statistics are collected for landings of individual Sepia species. 92 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Sepietta oweniana Common bobtail Cephalopod biology and fisheries in Europe: II. Species Accounts 9 | 93 Sepietta oweniana (d’Orbigny, 1841) Paola Belcari, Uwe Piatkowski, Paolo Sartor, Evgenia Lefkaditou, Graham J. Pierce, A. Louise Allcock, and Patrizia Jereb Common names Sépiole commune (France), Είδος σεπιέττας [eidos sepiettas] (Greece), seppiola comune (Italy), chopo-anão (Portugal), sepieta comùn (Spain), common bobtail squid (UK) (Figure 9.1). Synonyms Sepiola petersii Steenstrup, 1887, Sepiola scandica Steenstrup, 1887, Sepiola oweniana d’Orbigny, 1841. 9.1 Geographic distribution The common bobtail squid, Sepietta oweniana (d’Orbigny, 1841), lives in the Northeast Atlantic from Norway south to Mauritania and throughout the Mediterranean to the Sea of Marmara (Reid and Jereb, 2005) (Figure 9.2). In the Northeast Atlantic, it extends from the west coast of Norway as far north as off Alesund (62°45’N; Grieg, 1933), and is regularly encountered in the Skagerrak and Kattegat (Hornbörg, 2005). It is recorded off the Faroe Islands (Nielsen, 1930) and is widely distributed along the coast of Scotland and in Irish waters Figure 9.1. Sepietta oweniana. Dor(Massy, 1928; Stephen, 1944), the Porcupine sal view. From Muus (1963). Seabight (southwestern Ireland; Collins et al., 2001), and the Celtic Sea (Lordan et al., 2001a). It is recorded in the North Sea (De Heij and Baayen, 2005; Oesterwind et al., 2010) and extends south along the French and Spanish coasts to Morocco and south to 14°N (Guerra, 1992). Sepietta oweniana is widely distributed throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Guescini and Manfrin, 1986a; Krstulović Šifner et al., 2005), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b). The species has been recorded also in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). 94 | ICES Cooperative Research Report No. 325 Figure 9.2. Sepietta oweniana. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 9.2 Taxonomy 9.2.1 Systematics Coleoidea – Decapodiformes –– Sepiolidae – Sepiolinae – Sepietta. 9.2.2 Type locality Not designated : “…nous ignorons entièrement d’où ils viennent…” [d’Orbigny, in Férussac and d’Orbigny, 1834–1948 (1841): 230]. 9.2.3 Type repository Originally Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France; specimen not extant [fide Lu et al., (1995: 322)]. 9.3 Diagnosis 9.3.1 Paralarvae This species does not have paralarvae sensu Young and Harman (1988). Hatching size varies between 2.5 and 5 mm ML (Naef, 1921/1923; Mangold-Wirz, 1963a; Bergström and Summers, 1983; Cuccu et al., 2010). Although measurements taken on live specimens may give larger values than measurements taken on fixed specimens (e.g. 3– 5 mm ML; Bergström and Summers, 1983, vs. 2.5 mm ML; Naef, 1921/1923), this is unlikely to account for all the above-mentioned variability. Cephalopod biology and fisheries in Europe: II. Species Accounts 9.3.2 | 95 Juveniles and adults: Figure 9.3. Sepietta oweniana. Dorsal view. Photo: Evgenia Lefkaditou. Sepietta oweniana (Figure 9.3) is a small species. A maximum ML of 45 mm for females (Ciavaglia and Manfredi, 2009) and 35 mm for males (e.g. Mangold-Wirz, 1963a; Salman, 1998; Sartor et al., 1998b) was reported for the Mediterranean Sea. However, a larger size of 50 mm is reported for an unsexed specimen from the North Sea (Bergström and Summers, 1983), and a record of 52 mm exists for an unsexed specimen from the northeastern Ionian Sea (Lefkaditou et al., 2003a). The mantle is domeshaped, more rounded in females, posteriorly. Fins are wide, rounded, and semi-circular, with pronounced anterior lobes, or ”earlets”; they do not extend beyond the mantle either anteriorly or posteriorly. Arm suckers are biserial. Figure 9.4. Sepietta oweniana. (a) typical hectocotylus: A, four basal suckers; H, copulatory apparatus; B, first couple of enlarged suckers; C, two – four smaller suckers; D, second couple of enlarged suckers; E, distal smaller suckers. From Cuccu et al., (2009a). (b) bursa copulatrix. Photo: Evgenia Lefkaditou. (a) (b) In males, the proximal ends of arms I are fused; the first left dorsal arm is hectocotylized with a modification affecting the basal portion of the arm and the dorsal series of suckers. At the base of that arm, there are normally 4 basal suckers, followed by a typical fleshy hook, the copulatory apparatus. In the dorsal series of suckers on this modified arm, two conspicuously enlarged suckers are followed distally by 2–4 smaller suckers, then another 2 larger suckers; the remaining suckers decrease in size towards the distal tip of the arm (Figure 9.4). The ventral series bears moderately enlarged suckers, and the oral surface of the modified region is broadly concave. The copulatory apparatus consists of a fleshy transverse swelling with a long, hook-like, inwardly curved horn, and a deep cleft medially over a flask-like rugose bulb, swelling at the dorsal edge. The female bursa copulatrix (Figure 9.4) is very large and extends posteriorly beyond the gill insertion. 96 | ICES Cooperative Research Report No. 325 Figure 9.5. Sepietta oweniana. Tentacular club. Photo: Evgenia Lefkaditou. The tentacular clubs (Figure 9.5) are long and well-developed, with 16–32 suckers in transverse rows; all the suckers are of similar (minute) size, giving the club surface a velvety appearance. Light organs are absent. The animal’s colouration is reddish brown, with many iridescent gradations, especially on the dorsal side (Naef, 1921/1923; Guerra, 1992; Reid and Jereb, 2005). 9.4 Remarks Six specimens were reported from Visakhapatam waters (Bay of Bengal, Indian Ocean) by Mohan and Rao (1978). However, no other records of the species in the Indian Ocean exist. Intraspecific variability in the number of suckers at the base of the hectocotylus has been reported for the populations of the Ligurian Sea (Orsi Relini and Bertuletti, 1989), Sardinian waters (Cuccu et al., 2009a), and the Sicilian Channel (Jereb and Di Stefano, 1995; Jereb et al., 1997a). A variation from the usual number of 4 basal suckers was observed in one specimen off Mola di Bari (southern Adriatic Sea; Bello, 1995a); however, in that case, the hectocotylus appeared to have been truncated and then regenerated. Also, anomalous hectocotyli, differing from the typical structure, have been observed in Sicilian and Sardinian populations (Jereb et al., 1997a; Cuccu et al., 2009a), and a double hectocotylization has been reported for a specimen of the Sicilian population (Jereb et al., 1997a). To date, it is not clear whether these anomalous hectocotyli are functional, something which would be particularly interesting to ascertain, because of the supposed morphological correlation between the hectocotylus and the bursa copulatrix. The high percentage of variants observed within mature animals would indicate that sexual maturity is not affected by such malformations. Observations from the Sardinian populations indicate that the phenomenon is not limited to mature animals, but that it also occurs in immature specimens (Cuccu et al., 2009a). Similar variability has been described for Sepiola atlantica (Guerra, 1986), in which it has been attributed to high genetic plasticity. In his recent review of the nomenclature in the genus Sepietta, Bello (2011) demonstrated that both binomina Sepiola petersii Steenstrup, 1887 and Sepiola scandica Steenstrup, 1887 are junior synonyms of Sepietta oweniana (d’Orbigny, 1841). It has recently been clarified that the first “written” description of S. oweniana and the first “illustrated” description appear in different sections of the major work produced by Férussac and d’Orbigny (1834-1848) (Groenenberg et al., 2009; Bello, 2011). It has been noted that the text of Férussac and d’Orbigny was issued in 10 “livraisons” (Tillier and Boucher-Rodoni, 1993, p. 100) and that each provide the date of publication of each book. Based on this evidence, the correct date of publication of the species is 1841, the written description (published in 1841) having priority over the illustrated one (published in 1842) (Art. 21.6 of the International Commission on Zoological Nomenclature, 1999) (Bello, 2011). Cephalopod biology and fisheries in Europe: II. Species Accounts | 97 Sepietta oweniana and S. neglecta females are similar in external appearance, and the character currently used to discriminate sepiolid females, i.e. the bursa copulatrix, is also identical in these two species (Bello, 1995b), making it very difficult to distinguish between them at small size (S. oweniana is larger). According to Naef (1921/1923) and others (e.g. Guerra, 1992; Bello, 1995b; Lefkaditou and Kaspiris 1996; Reid and Jereb, 2005), the only difference between the two species is in the tentacular clubs, which are smaller, more delicate, and bear fewer suckers in S. neglecta. According to Lefkaditou and Kaspiris (1996), club-length indices can be used to discriminate the two species. 9.5 Life history Lifespan appears to be 6–12 months. Hatchlings apparently initially adopt a planktonic-necktobenthic mode of life. Animals mature at 4–5 months of age, and spawning takes place year–round, but with regionally varying seasonal peaks. 9.5.1 Egg and juvenile development The eggs are spherical to lemon-shaped and greyish-white in colour (Figure 9.6). The average egg size at laying varies between 2.4 and 3 mm (larger diameter; MangoldWirz, 1963a; Bello and Deickert, 2003; Cuccu et al., 2010), but the eggs swell during embryonic development to ca. 5.0–5.7 mm (Mangold-Wirz, 1963a; Cuccu et al., 2010). Eggs are released during several spawning events onto various solid substrata, both living and dead, with a preference for ascidians (Microcosmus spp) in the Catalan Sea (Mangold-Wirz, 1963a; Deickert and Bello, 2005). The egg envelope was described as “thin and elastic” by Mangold-Wirz (1963a), although hard egg envelopes have subsequently been observed in egg clutches from the Catalan Sea (A. Deickert, pers. comm.). Similarly, eggs in a clutch found 544 m deep by Cuccu et al. (2010) were covered by a hard shell, as is typical for other sepiolids that spawn at depths of 500–600 m (e.g. Rossia macrosoma; Mangold-Wirz, 1963a). The number of eggs in wild-collected egg clutches available from the literature is reported in Table 9.1. The overall number of eggs lies within the range of eggs spawned in aquarium studies, i.e. between 2 and 176 (see Bergström and Summers, 1983; Bello and Deickert, 2003), with median values between 30 and 50. It has been suggested that unusually large clutches from the field may result from more than one Figure 9.6. Sepietta oweniana. Egg clutch. From Cuccu et spawning event by the same feal. (2010). male or from several females spawning on the same piece of substratum (Mangold-Wirz, 1963a; Deickert and Bello, 2005). 98 | ICES Cooperative Research Report No. 325 Table 9.1. Sepietta oweniana. Number of clutches (Nc), number of eggs (or range) (Ne), and clutch size (CS, mean number of eggs) as observed in egg clutches collected from the sea (modified from Deickert and Bello, 2005). Region Nc Nc CS Reference Kattegat 1 130 - Thorson (1946) Skagerrak 4 32–103 53.25 Bergström and Summers (1983) - 30–60 - Mangold-Wirz (1963a) 89 3–62 23.91 Bello and Deickert (2003) Northeast Atlantic Mediterranean Sea Catalan Sea The duration of egg development is highly dependent on water temperature. Data from the literature indicate incubation times of 25 d at 23°C (Jecklin, 1934, in MangoldWirz, 1963a), 30 d at 20°C (Mangold-Wirz, 1963a), 2–3 months at ≥10°C, and 6 months at 6.8°C (Bergström and Summers, 1983). Embryo and hatchling are illustrated in Figure 9.7. The only information available on S. oweniana juvenile behaviour comes from aquarium- based observations by Bergström and (b) (a) Summers (1983). Figure 9.7. Sepietta oweniana. (a) embryo, (b) newly hatched animal. Newly hatched From: Cuccu et al. (2010). individuals take shelter on the bottom and do not start feeding until they are ca. 1 day old. They then actively search for food day and night, swim freely to catch their prey, and spend short periods on the bottom. This planktonic-nektobenthic life strategy gradually changes with age, and they eventually spend more time on the bottom or buried in the sand. At ca. 10 weeks of age, they settle into a diurnal activity pattern, spending daylight buried in the sand and emerging to feed at night (Bergström and Summers, 1983). In rearing experiments, food was given once a day consisting mainly of juvenile shallow-water crustaceans. Juvenile S. oweniana preferred mysids of ca. 0.5–0.67 of their own body length, but were occasionally seen capturing prey their own size. Because the spawning period extends year-round and the growth rate is fast, recruitment is nearly continuous, and several cohorts succeed one another. Consequently, it is difficult to identify different cohorts (D’Onghia et al., 1995; Sartor et al., 1998b). 9.5.2 Growth and lifespan Growth after hatching seems relatively independent of water temperature and is quite rapid. Studies in the laboratory report an average growth rate of 4–8 mm month–1, with slightly faster growth rates in females (5.3 mm month–1 on average vs. 4.2 mm month– 1 in males; Bergström and Summers, 1983). However, recent observations by Giordano et al. (2009) on samples from the southern Tyrrhenian Sea indicated no significant difference in growth rate between males and females. Putative age estimates based on Cephalopod biology and fisheries in Europe: II. Species Accounts | 99 statolith reading suggest an age of ca. 4.5–6 months for mature and spent females and 5–5.5 months for mature males from southern Portuguese coasts (Czudaj et al., 2012). Based on this information, animals grow and mature within 6–7 months of hatching. The whole life cycle, therefore, would be completed between 6 months and one year, depending mainly on the duration of embryonic development (Boletzky, 1975b; Mangold and Froesch, 1977; Bergström and Summers, 1983). Length–weight relationships are summarized in Table 9.2 below. Table 9.2. Sepietta oweniana. Length–weight relationships in different geographic areas for females (F) and males (M). Original equations were converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Southern Tyrrhenian Sea 0.225 1.61 F Giordano et al. (2009) 0.344 1.29 M 1.0019 1.97 F 0.905 2.12 M Northern Aegean Sea 9.5.3 Lefkaditou et al. (2007) Maturation and reproduction Sex ratios have been observed to differ from 1:1 in some areas, both in the Atlantic and in the Mediterranean. A slight predominance of females over males was reported in the Catalan Sea (Mangold-Wirz, 1963a), whereas a slight predominance of males over females has been reported for the Skagerrak (Bergström and Summers, 1983), the northern Tyrrhenian Sea (Sartor et al., 1998b), Sardinian waters (Cuccu et al., 2010), and the Strait of Sicily (Jereb et al., 1997b). Males mature smaller than females, although size at first maturity and size at 50% maturity are variable in both sexes, throughout the distributional range (Table 9.3). Size at 50% maturity shows a similar degree of variability in both sexes and is comparable among the different Mediterranean populations, except for the Catalan Sea, where it appears that mature females are larger. Again, with the exception of the Catalan Sea, females in the Atlantic mature at a slightly larger size than females in the Mediterranean. However, as noted by Cuccu et al. (2010), it is possible that females from the Catalan Sea carrying “large” oocytes had already spawned their “smooth” oocytes before being captured and examined. If this is the case, size at maturity of females from the Catalan Sea would probably be comparable with data from other Mediterranean areas. Mature animals are found throughout the year both in the Northeast Atlantic and in the Mediterranean, suggesting almost continuous spawning for this species (e.g. Mangold-Wirz, 1963a; Bergstom and Summers, 1983; Belcari and Sartor, 1999b; Reid and Jereb, 2005; Czudaj et al., 2012). Peaks in reproductive activity, however, are reported in both areas for females. In the Northeast Atlantic, peaks have been documented in March and August–November for Gullmar Fjord (Skagerrak, Northeast Atlantic; Bergström and Summers, 1983), and in early summer and autumn–winter (maximum in February) for Portuguese waters (Czudaj et al., 2012). 100 | ICES Cooperative Research Report No. 325 Table 9.3. Sepietta oweniana. Data on sexual maturity for females (F) and males (M) and potential fecundity (PF) in females, as available from the literature; MLm min, mantle length of the smallest mature specimens; MLm50, mantle length at 50% sexual maturity. Modified from Cuccu et al. (2010). Region Sex ML MLm- MLm50 PF Reference min Northeast Atlantic Gullmar Fjord Portuguese F - - 33 130 Bergström and M - - 23 - Summers (1983) F 14.0– 20.1 24.4 18– Czudaj et al. 616 (2012) 150– Mangold-Wirz 200 (1963a) waters 36.0 M 14.0– 13.4 20.8 30 >35 28.0 Mediterranean Sea Catalan Sea F 20.0– 40.0 M 20.0– * - - 643–1 Bello and Deickert 185 (2003) - Orsi Relini and Ber- 35.0 “ F 16.5– 24.5 38.5 Ligurian Sea F 10.0– 20 - 35.0 M 14.0– tuletti (1989) 18 - - 13.0– 19 26 - Sartor et al. 40.0 15 21 - (1998b) 30.0 Northern Tyr- M rhenian Sea 14.0– 35.0 Southern Tyr- F 18.0– 24 24 60– Giordano et al. rhenian Sea M 34.0 18 18 106 (2009) - 15.0– 29.0 Sardinian seas F 12.9– 18.5 24 30.8 M 13.4– 14.3 20 18 - 45– Cuccu et al. 263 (2010) 29.1 Strait of Sicily F 14.5– - 36.8 M 14.0– Jereb et al. (1997b] 14 - - 34.0 Adriatic Sea Aegean Sea F - 24 - - Guescini and M - 17 - - Manfrin (1986a) F 14.0– 22 28 58– Salman (1998) 36.0 M 18.0– 236 21 35.0 * 75% of male specimens were mature at 20 cm ML. 24 - Cephalopod biology and fisheries in Europe: II. Species Accounts | 101 In the Mediterranean, peaks of reproductive activity are recorded in May–September in the Catalan Sea (western Mediterranean; Mangold-Wirz, 1963a), in July in the northern Tyrrhenian Sea (central Mediterranean; Sartor et al., 1998b), in winter (February– March) in the Strait of Sicily (central Mediterranean; Jereb et al., 1997b), and in March– April and November in the Aegean Sea (Salman, 1998; Lefkaditou and Kaspiris, 2005). Spawning is usually in relatively shallow coastal water, although records exist of egg masses in deeper waters (down to 544 m; Cuccu et al., 2010). Several sequential egglaying events have been observed in aquaria by Bello and Deickert (2003), who, combining these observations with the examination of ovaries, concluded that S. oweniana can be considered a “small-size multiple spawner”, which continues to feed and grow during the spawning phase. The same conclusion was reached by Cuccu et al. (2010). The main features of this life strategy are the continuous production and ripening of oocytes, and the continuous laying of egg batches over an extended period of time. These results would support the hypothesis that females from the Catalan Sea with “large” eggs, reported by Mangold-Wirz (1963a), may indeed have been mature females that had already spawned their “smooth” eggs. Recent observations from Portuguese waters (Czudaj et al., 2012) report females with potential fecundity values higher than those recorded in other areas of the species’ distribution range. However, the highest potential fecundities for this species are those recorded by Bello and Deickert (2003) for wild-caught females from the Catalan Sea kept in an aquarium (Table 9.3). Mating takes place head-to-head and is a rather quick and violent event (e.g. MangoldWirz, 1963a; Bergström and Summers, 1983). Spermatophores are placed inside the female’s mantle cavity, on the bursa copulatrix area, where spermatangia are stored. 9.6 Biological distribution 9.6.1 Habitat Sepietta oweniana is a demersal species, living within a wide depth range from 20 m down to >1000 m (i.e. 1027 m, R. Villanueva, unpublished data in Guerra, 1992). In the Northeast Atlantic, it is most common between 50 and 300 m (Bergström and Summers, 1983; Collins et al., 2001), but also occurs on the upper slope (between 300 and 500 m) in the Gulf of Cádiz and in southern Portuguese waters (Silva et al., 2011; Czudjac et al., 2012). In the Mediterranean, major concentrations are most frequent between 200 and 400 m, near the shelf break (Lumare, 1970; Bello and Motolese, 1983; Guescini and Manfrin, 1986a; Belcari et al., 1989a; D’Onghia et al., 1995; Villanueva, 1995b; Jereb et al., 1997b; Quetglas et al., 2000; González and Sánchez, 2002; Lefkaditou et al., 2003a; Lefkaditou and Kaspiris, 2005; Ciavaglia and Manfredi, 2009; Giordano et al., 2009; Guijarro et al., 2011). In some areas and seasons (e.g. in the Ligurian Sea and the northern Tyrrhenian Sea), major concentrations have been reported between 400 and 500 m (Orsi Relini and Massi, 1988; Orsi Relini and Bertuletti, 1989; Mannini and Volpi, 1989), but in other areas (e.g. in the Gulf of Naples and the Adriatic Sea), the species has been reported to be more abundant in shallower water (Naef 1921/1923; Mangold-Wirz, 1963a; Soro and Piccinetti Manfrin, 1989; Ciavaglia and Manfredi, 2009). Sepietta oweniana prefers soft, muddy substrata throughout its range. It is often found on fishing grounds for Norway lobster (Nephrops norvegicus) and shrimp and is very frequently associated with Rondeletiola minor (e.g. Naef 1921/1923; Mannini and Volpi, 1989; Belcari et al., 1989a; Bello et al., 1994; Villanueva, 1995b; Jereb et al., 1997b; González and Sánchez, 2002; Lefkaditou and Kaspiris, 2005; Ciavaglia and Manfredi, 2009). 102 | ICES Cooperative Research Report No. 325 Sepietta oweniana is found regularly in the Kattegat and Skagerrak between the eastern North Sea and the brackish western Baltic Sea (Bergström and Summers, 1983; Hornbörg, 2005). However, its tolerance to salinity variations seems to be lower than in other bobtail squid, because it has never been found in brackish waters (Katağan et al., 1993; Ünsal et al., 1999). 9.6.2 Migrations Seasonal movements related to reproduction and vertical movements, mostly linked to trophic relationships, have been reported for this species in several geographic areas, both in the North Atlantic and in the Mediterranean Sea (Mangold-Wirz, 1963a; Bergström and Summers, 1983; Orsi Relini and Bertuletti, 1989; Mannini and Volpi, 1989; Lefkaditou and Kaspiris, 2005). However, no similar movements have been observed in other areas, such as in the northern Aegean Sea and the Strait of Sicily (D’Onghia et al., 1996; Jereb et al., 1997b), possibly because the continental shelf is narrower in those areas. 9.7 Trophic ecology 9.7.1 Prey The food spectrum of S. oweniana is mainly crustaceans, mostly mysids, euphausiids, and decapods, but fish also seem to constitute a conspicuous fraction of the natural diet (Orsi Relini and Massi, 1988). Cannibalism has been observed in aquarium studies, and cephalopod remains (belonging mainly to the Sepiolidae) were found in the stomachs of wild-caught specimens (Orsi Relini and Massi, 1988). Specific preferences for the euphasiid Meganyctiphanes norvegica in North Atlantic waters (Bergström, 1985) and the decapod Pasiphaea sivado in the Ligurian Sea (Orsi Relini and Massi, 1988) have been observed (Table 9.4), consistent with the existence of trophic migrations in response to prey abundance and distribution. Sepietta oweniana has been successfully cultured in aquaria (Bergström and Summers, 1983; Bergström, 1985), fed on mysids (Praunus flexuosus and P. inermis), amphipods (Ericthonius), and large copepods. Adults fed on Praunus flexuosus and the shrimps Palaemon elegans, Thoralus cranchii, and Crangon crangon. According to aquarium observations (Bergström, 1985), the prey-attack system and actual prey capture are essentially visual, as observed for S. officinalis (Messenger, 1968) and for other species of Sepiolinae (Boletzky et al., 1971; Boletzky, 1975b). Observations of hatchlings and juveniles attacking air bubbles and floating particles suggest that prey capture is initially indiscriminate (Bergström, 1985). Individuals are able to catch prey of considerable size, even animals larger than themselves (Bergström, 1985). Adults feed at very low light intensity (Bergström, 1985); dusk and dawn are probably the main periods of feeding in the natural environment (Boletzky, 1975b). Cephalopod biology and fisheries in Europe: II. Species Accounts | 103 Table 9.4. Prey composition of Sepietta oweniana, as known from studies in the Northeast Atlantic (Bergström, 19851) and the Mediterranean Sea (Orsi Relini and Massi, 1988 2; Vafidis et al., 20093). Taxon Species Osteichthyes indet.2,3 Crustacea Decapoda Pleocyemata-Caridea Pandalidae indet.1, Pasiphaea sivado2 Pleocyemata-Brachy- indet.3 ura Amphipoda indet.3 Euphausiacea Meganyctiphanes norvegica1,2, indet.2 Mysida indet.2,3 Peracarida Isopoda indet.2, Natatolana borealis (as Cirolana borealis)2 Cephalopoda indet.2, Solenogastres indet.3, Mollusca Echinodermata Crinoidea Leptometra spp.2 Cnidaria Anthozoa indet.3 Polychaeta indet.3 9.7.2 Predators Sepietta oweniana is potentially available to all benthic and demersal predators of the continental shelf and slope, and is eaten mostly by fish of medium and large size, but also by cetaceans and crustaceans (Table 9.5). It seems particularly vulnerable to some species of elasmobranch (Sartor, 1993; Bello, 1997). Table 9.5. Known predators of Sepietta oweniana in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Crustacea Giant red shrimp (Aristaeomorpha Bello and Pipitone (2002) foliacea) Deep-water rose shrimp (Para- Sobrino et al. (2005) penaeus longirostris) Cephalopoda Common cuttlefish (Sepia offici- Alves et al. (2006) nalis) Musky octopus (Eledone mos- Krstulović Šifner and Vrgoč (2009b) chata) Chondrich- Black-mouthed dogfish (Galeus Macpherson (1981), Kabasakal thyes melastomus) (2002), Fanelli et al. (2009) Kitefin shark (Dalatias licha) Matallanas (1982) Lesser spotted dogfish (Scyliorhi- Macpherson (1981) nus canicula) Rabbit fish (Chimera monstrosa) Bello (1997) Smooth lanternshark (Etmopterus Xavier et al. (2012) pusillus) Thornback ray (Raja clavata) Kabasakal (2002), Šantić et al. (2012) Velvet belly lanternshark Macpherson (1981), Sartor (1993), (Etmopterus spinax) Neiva et al. (2006) 104 | ICES Cooperative Research Report No. 325 Osteichthyes Atlantic cod (Gadus morhua) Bergström and Summers (1983) Blue-mouth (Helicolenus dacty- Neves et al. (2011) lopterus) European hake (Merluccius mer- Carpentieri et al. (2000, 2005) luccius) Haddock (Melanogrammus ae- Bergström and Summers (1983) glefinus) Cetacea Swordfish (Xiphias gladius) Salman (2004) Common dolphin (Delphinus del- Santos et al. (2004a, 2013) phis) Harbour porpoise (Phocoena Börjesson et al. (2003), Santos et al. phocoena) (2005b) Harbour seal (Phoca vitulina) Brown et al. (2001) Striped dolphin (Stenella coerule- Würtz and Marrale (1993) oalba) 9.8 Other ecological aspects Studies carried out on the demersal community structure of the western Mediterranean (Biagi et al., 2002) reported a species assemblage recurrent off the western central Italian coasts from 200 to 450 m. Sepietta oweniana plays an important role in this faunistic assemblage, both in terms of frequency of occurrence and in percentage abundance; there, the species was found associated with Norway lobster (Nephrops norvegicus), European hake (Merluccius merluccius), and greater forkbeard (Phycis blennoides). 9.9 Fisheries Sepietta oweniana is one of the most abundant bobtail squid throughout its distributional range and one of the most abundant cephalopods caught in some Mediterranean areas (Reid and Jereb, 2005). It represents an important bycatch of many trawl fisheries, both multispecies fisheries and those targeting shrimp. In southern Sicilian waters a targeted fishery exists for sepiolids (Jereb et al., 1997b). Specific statistics are not available, but the species is commonly sold in Mediterranean markets and is valued as a delicacy in areas such as southern Sicily. In the Mediterranean, catches are generally most abundant in summer, and a marked seasonality has been observed in some areas (e.g. the northern Tyrrhenian Sea; Belcari et al., 1998). 9.10 Future research, needs, and outlook Important topics for future research include the separation of stocks and cohorts. In particular, additional studies on the Catalan population may help in better understanding maturation strategies and clarifying values for size at maturity that look anomalous in comparison with those recorded for other Mediterranean populations. In order to understand the effect of fishing pressure on the species, it is essential that fishery landings are identified to species. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Sepiola atlantica Atlantic bobtail | 105 106 | 10 ICES Cooperative Research Report No. 325 Sepiola atlantica d’Orbigny, 1842 Ángel Guerra, Graham J. Pierce, Lee C. Hastie, A. Louise Allcock, Evgenia Lefkaditou, and Patrizia Jereb Common names Sépiole grandes oreilles (France), chopoanão (Portugal), sepiola atlántica (Spain), Atlantic bobtail squid (UK) (Figure 10.1). Synonyms None. 10.1 Geographic distribution The Atlantic bobtail squid, Sepiola atlantica d’Orbigny, 1842, is found in the Northeast Atlantic from ca. 65 to 35°N (Reid and Jereb, 2005) (Figure 10.2). Its distribution extends from Iceland (Degner, 1925; Adam, 1939; Bruun, 1945) and the Faroe IsFigure 10.1. Sepiola atlantica. Dorsal view. lands (Nielsen, 1930) to the Norwegian Sea From Guerra (1992). and the west coast of Norway (Grimpe, 1925; Grieg, 1933; Jaeckel, 1958). Old records from the Skagerrak and Kattegat (Grimpe, 1925) are confirmed by recent information (Hornbörg, 2005), and incursions into the western Baltic Sea have been reported (Grimpe, 1925). Widely distributed and very common in the North Sea (Russell, 1922; Grimpe, 1925; Adam, 1933; Gittenberger and Schrieken, 2004; De Heij and Baayen, 2005; Oesterwind et al., 2010), it extends along the north and west coasts of Scotland (Russell, 1922; Stephen, 1944), through Irish and British waters (Massy, 1928; Lordan et al., 2001a), the Porcupine Seabight (southwestern Ireland; Collins et al., 2001), and the Celtic Sea (Lordan et al., 2001a). From the English Channel (Pfeffer, 1908; Grimpe, 1925), it extends south along the west coasts of France and Spain (Guerra, 1992) to Northwest Africa off the Moroccan coast (as far as due west of Casablanca; Robson, 1926). A single record from the Mediterranean Sea has never been confirmed (Würtz et al., 1995). Cephalopod biology and fisheries in Europe: II. Species Accounts | 107 Figure 10.2. Sepiola atlantica. Geographic distribution in the Northeast Atlantic. 10.2 Taxonomy 10.2.1 Systematic Coleoidea – Decapodiformes –– Sepiolidae – Sepiolinae –Sepiola. 10.2.2 Type locality Bay of Biscay, France. 10.2.3 Type repository Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France; syntype 2-1-1209 [fide Lu et al. (1995)]. 10.3 Diagnosis 10.3.1 Paralarvae The size of individual hatchlings obtained in the laboratory ranges between 1.1 and 1.7 mm (Rodrigues et al., 2011a). In Galician waters (northwestern Spain), they range from 1.5 to 2.0 mm ML and have been collected in midwater both night and day. Paralarvae are similar to adults except for their shorter arms and tentacles in relation to mantle length (Á. Guerra, pers. comm.). 10.3.2 Juveniles and adults Recent observations on populations around Anglesey (north Wales; Jones and Richardson, 2012) and from the Ría de Vigo (Galicia, northwestern Spain; Rodrigues et al., 2011b) recorded maximum mantle length as 24 mm for females, larger than previously reported for the species (i.e. 21 mm; Yau and Boyle, 1996; Reid and Jereb 2005). Adult males and females are of similar size. Fins are short and do not exceed mantle length anteriorly or posteriorly. Arms IV bear biserial suckers proximally, and 4–8 rows of 108 | ICES Cooperative Research Report No. 325 minute suckers at the distal tips; the remaining arms bear two series of suckers throughout. The dorsal left arm is modified (hectocotylized) in mature males (Figure 10.3) and strongly bent in its distal half; it is characterized by the presence of a fleshy pad formed from enlarged and fused sucker pedicels, and a copulatory apparatus formed by a large swollen horn, with secondary lobes, basally. In the dorsal series of suckers, distal to the copulatory apparatus, there are 3–4 slightly enlarged suckers with swollen pedicels, followed by 3–4 greatly reduced suckers, then by 3–5 greatly enlarged suckers, ca. halfway along the arm. Tentacular clubs bear 8 longitudinal series of suckers, arranged in transverse rows; suckers in the dorsal series are larger than those in the ventral ones. Mature females do not have a “muscle constrictor” and have a small bursa copulatrix. Paired, kidney-shaped light organs (photophores) are present inside the mantle cavity on each side of the ink sac (Guerra, 1992; Bello, 1995b; Reid and Jereb, 2005). There is a dimorphism in the brachial crown in mature individuals, with males having a muscular nodule at the base of the ventral arms (Rodrigues et al., 2012). Figure 10.3. Sepiola atlantica. Hectocotylized arm. From Guerra (1992). 10.4 Remarks A single record of S. atlantica in the Mediterranean Sea exists (Würtz et al., 1995). However, the presence of this species has not otherwise been reported there, either before or since (e.g. Bello 1986, 1992a, 2004; Mangold and Boletzky, 1987; Salman, 2009); therefore, that record is likely a misidentification. The subfamily Sepiolinae, to which Sepiola belongs, can be distinguished from other subfamilies in the Sepiolidae by several features: the anterior edge of the mantle does not cover the funnel ventrally and is fused with the head dorsally by a cutaneous occipital band that occupies from 33 to 50% of the head width. Unlike other genera within the subfamily Sepiolinae, Sepiola species have a pair of kidney-shaped light organs (photophores) inside the mantle cavity, over the ink sac. Sepietta species do not have photophores, and in Rondeletiola, the light organ is large and round, being formed by the fusion of the two organs (Guerra, 1992; Bello, 1995b; Reid and Jereb, 2005). Recent molecular data (Groenenberg et al., 2009) highlighted the presence of an additional species of sepiolid in the North Sea, now described as Sepiola tridens De Heij and Goud, 2010, which is closely related to S. atlantica. In their study, Groenenberg et al. (2009) found that some one-third of samples they originally identified as S. atlantica formed a separate well-supported clade in a phylogenetic tree constructed from Bayesian inference analysis of the mitochondrial gene cytochrome oxidase subunit I (COI: the ”barcode of life” gene). The molecular data suggested that members of this clade, now described as S. tridens, were more closely related to S. atlantica than to any of the other Sepiola species in the North Sea, a fact supported by their morphological similarity. However, despite the similarity, De Heij and Goud (2010) identified differences in the tentacular club (length <7 mm in adult S. tridens vs. >7 mm in adult S. atlantica; 6 club sucker rows in S. tridens vs. 8 club sucker rows in S. atlantica), in the hectocotylus (5–8 large suckers on the crest before the tip in S. tridens vs. 3–4 in S. atlantica) and in Cephalopod biology and fisheries in Europe: II. Species Accounts | 109 body patterning (light pink base colour with a strong honeycomb pattern of chromatophores on the dorsum of S. tridens vs. a whitish base colour with a less strong pattern on dorsum in S. atlantica). The S. tridens used in the molecular study were captured in slightly deeper water (S. tridens 43–94 m, S. atlantica 19–68 m; Groenenberg et al., 2009). A preliminary analysis of additional trawl data confirmed the difference; the average capture depth for S. tridens was 81.8 m vs. 37.4 m in S. atlantica (De Heij and Goud, 2010). Subsequent data (De Heij and Goud, 2010) show that S. tridens is also present in much deeper water 250 km west of Ireland. De Heij and Goud (2010) report S. tridens from the North Sea, the Skaggerak, the English Channel, the Celtic Sea, southwestern Ireland, deep water west of Ireland, and off northwestern Spain. It is possible that some records of S. atlantica actually pertain to S. tridens, although De Heij and Goud (2010) confirm that the populations in Firemore Bay (Yau and Boyle, 1996) and Ría de Vigo (various authors) likely do pertain to S. atlantica. Sepiola tridens has been identified genetically in samples collected off the Portuguese shelf at night at bottom depths of 100– 148 m. Its presence off the Portuguese coast increases its southern geographic limit to 41°23’N (Roura, 2013). 10.5 Life history An intermittent terminal spawner, S. atlantica spawns year-round with peaks in summer and autumn. Hatchlings resemble adults, but have a brief pelagic phase. Lifespan probably varies between 7 and 10 months. 10.5.1 Egg and juvenile development Eggs are laid singly, but attached close together in clusters to hard structures on the seabed, including hydroids and bryozoans (e.g. Cellaria spp.) (Rees, 1957; Rodrigues et al., 2011c). Eggs are spherical, with a slightly pointed apical tip, resulting in a typically droplet-like shape. In an aquarium-based study, the major axis of egg capsules ranged in length between 1.75 and 4.92 mm (mean 2.75 ± 0.44 mm; Rodrigues et al., 2011c). The duration of embryonic development determined in aquaria is strictly dependent on water temperature, varying from 61.8 (± 3.8) d at 13°C, to 40.1 (± 4.8) d at 16.4°C, and 22.6 (± 1.7) d at 18°C (Rodrigues et al., 2011a). The percentage of eggs that successfully hatch varies from 98.5 to 100%. Newly hatched paralarvae measure 1.1–1.7 mm (1.5 ± 0.3 mm) ML. Total length ranges between 2.6 and 3.6 mm (3.2 ± 0.5 mm), and body weight between 0.077 and 0.098 g (0.081 ± 0.02 g). There are no relationships between hatchling body size and the duration of the embryonic phase, or between hatchling length and weight (Rodrigues et al., 2011a). Similar results were obtained by Jones and Richardson (2010), who recorded embryonic development duration of 33 d at 14.4°C. Newly hatched individuals measured 1.91 mm ML and entered a pelagic paralarval phase lasting 6 d. Some 10–20 days after hatching, the internal yolk sac was exhausted (Jones and Richardson, 2010). Recruitment occurs year-round, but peaks in spring, early summer, and autumn have been observed in Scottish and Galician waters (Yau, 1994; Yau and Boyle, 1996; Rodrigues et al., 2012). 10.5.2 Growth and lifespan Little information is available on S. atlantica growth. Measured as the increase in dorsal mantle length, growth recorded in aquaria consisted of two distinct phases: relatively slow during the first 120 d (ca. 0.05 mm d–1; 0.043 mm d–1 in males and 0.055 mm d–1 in females) and increasing slightly thereafter until day 210, when it levelled off (Jones and 110 | ICES Cooperative Research Report No. 325 Richardson, 2010). Limited data are available on length–weight relationships (Table 10.1). Table 10.1. Sepiola atlantica. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Only records from the ICES Area are included. Region a b Sex Reference West coast of Scotland 0.581 2.46 F Yau and Boyle (1996) 0.572 2.75 M 0.557 2.30 All North Sea Robinson et al. (2010) Rodrigues et al. (2013) reported regression equations to predict body weight and mantle length from measurements on the beaks of individuals sampled in the Ría de Vigo (both sexes combined): ln(BW) = 1.486 + 2.174 × ln(LRL and ln(ML) = 3.173 + 0.974 × ln(LRL) ln(BW) = 1.590 + 2.734 × ln(URL) and ln(ML) = 1.223 + 3.206 × ln(URL) where LRL is the lower rostral length (mm) and URL the upper rostral length (mm). The lifespan of S. atlantica likely varies between 7 and 10 months, depending on the duration of embryonic development, which, as noted above, is related to water temperature (Jones and Richardson, 2010). 10.5.3 Maturation and reproduction Yau and Boyle (1996) reported a sex ratio in animals of >10 mm ML (the sex of smaller animals could not be determined accurately) of ca. 1:1 in Scotland (ratio of males to females 1.4:1.0, n = 138). Rodrigues et al. (2011b) also reported that the sex ratio did not differ significantly from 1:1 in Galicia. Observations on the population in Loch Ewe (northwest coast of Scotland; Yau and Boyle, 1996) showed that MLm50% was ca. 13 mm in males and 16 mm in females. However, the mean body size of mature animals was similar in both sexes (ca. 15 mm). Mature animals were present from March to August, suggesting an extended spawning season, but with a peak in June for both sexes. The number of mature ova in females ranged between 42 and 126. Juvenile occurrence peaked in May, and no juveniles were recorded in March (Yau and Boyle, 1996). Similar results were obtained from studies of the population around Anglesey (north Wales; Jones and Richardson, 2012), where MLm50% was 13–14 mm in males and 16–17 mm in females. In the Ría de Vigo (northwestern Spain), however, S. atlantica matures smaller; the smallest mature males measured 8.05 mm ML, the smallest mature females 6.47 mm (Rodrigues et al., 2012), and MLm50% was 8.9 and 9.8 mm for males and females, respectively. Sepiola atlantica is an intermittent terminal spawner, with group-synchronous ovary maturation; it lays multiple eggs and deposits egg clutches in multiple locations (Rodrigues et al., 2011c). Examination of the ovaries has revealed that immature oocyte size varies between 0.03 and 3.75 mm (maximum diameter; Rodrigues et al., 2011c). Mature oocytes range in size between 1.57 and 5.42 mm (Rodrigues et al., 2012). The largest oocytes have been found in the largest females. The total number of eggs laid by a single female ranges between 31 and 115, and potential fecundity (i.e. the sum of the number of oocytes in Cephalopod biology and fisheries in Europe: II. Species Accounts | 111 the ovary and the oviducts plus the number of eggs already spawned) from 119 to 304 (Rodrigues et al., 2011c). The maximum number of spermatophores recorded in males is 1243 (Rodrigues et al., 2012), with a mean value of 369. Spermatophore length ranges from 3.31 to 9.23 mm. No significant relationship was observed between number of spermatophores and mantle length (Rodrigues et al., 2012). Mating behaviour has been studied in the laboratory (Rodrigues et al., 2009). There was no courtship in any of the mating events observed. The male moved quickly towards the female, holding her around the middle of the ventral mantle region with his arms. Positioned underneath the female, the male then introduced his pair of dorsal arms into the female‘s mantle cavity (the left dorsal arm is hectocotylized and transfers spermatophores), while grasping her ventral body with the laterodorsal pair of arms, and neck with the lateroventral pair, sometimes introducing these arms into the female‘s mantle cavity. Male colour remained constant throughout mating, whereas females slowly and continuously changed their chromatic patterns. Mating duration varied between 68 and 80 min (Rodrigues et al., 2009). 10.6 Biological distribution 10.6.1 Habitat Sepiola atlantica inhabits the continental shelf, its distribution extending to the edge of the slope. It can be considered a neritic species, occurring from the sublittoral zone to depths of 150 m. In Scottish waters, it is most common between 50 and 120 m (Yau, 1994; Yau and Boyle, 1996). In Iberian waters, it is commonly found from 6 to 50 m, as well as inside the Galician Rías (sheltered tectonic valleys), and it prefers clean sandy bottoms. It is epibenthic, but has been collected in midwater during both night and day (Collins et al., 2001). Bruun (1945) commented that most specimens recorded around Iceland were caught pelagically. The species is stenohaline and not found in areas with high salinity variation (Guerra, 1992; Rodrigues et al., 2011d). Collins et al. (2002), in their study on the distribution of cephalopods from plankton surveys around the British Isles, found that S. atlantica was the most abundant cephalopod in samples from the North Sea. 10.6.2 Migrations Seasonal migrations have been observed in the waters around Anglesey (north Wales; Jones and Richardson, 2012), where S. atlantica migrates inshore in July, reaching peak abundance between July and August, declining in numbers between September and October, and migrating offshore in late October. These movements are probably related to feeding strategies, because of the abundance of prey such as shrimps in shallow water in summer, and, more generally, to take advantage of environmental conditions favourable for enhanced growth and maturation. In addition, congregation in shallow waters may favour encounters with mates. Seasonal differences in abundance were also recorded in the Areamilla area (Galician waters, northwestern Spain; Rodrigues et al., 2011b), where, however, lowest abundance was recorded in summer. It was proposed that this seasonal pattern of abundance was due to migration of individuals from shallow to deeper waters, related to changes in bottom temperature. 112 | 10.7 ICES Cooperative Research Report No. 325 Trophic Ecology 10.7.1 Prey The main prey species of S. atlantica are mysids and decapod shrimps. Foraging primarily takes place at dawn and dusk, and prey are taken above the seabed (Yau, 1994). 10.7.2 Predators Sepiola atlantica is the most frequently recorded cephalopod in the diet of harbour porpoise in Scottish waters. The sepiolids are probably detected by porpoises directing their sonar into the substratum, detecting the acoustic signal given by the hole in which the animal lies (Santos and Pierce, 2003; Santos et al., 2004b). In Galician waters, the species has been recorded in the stomach contents of hake and gurnards (Á. Guerra, pers. comm.). Known predators of this species are listed in Table 10.2. Table 10.2. Known predators of Sepiola atlantica in the Northeast Atlantic. Taxon Species References Myxini Hagfish (Myxine glutinosa) Shelton (1978) Chondrich- Lesser spotted dogfish (Scyliorhi- Ellis et al. (1996) thyes nus canicula) Greater spotted dogfish (Scyliorhi- Ellis et al. (1996) nus stellaris) Osteichthyes Spotted ray (Raja montagui) Ellis et al. (1996) Spurdog (Squalus acanthias) Ellis et al. (1996) Thornback ray (Raja clavata) Ellis et al. (1996) Tope shark (Galeorhinus galeus) Ellis et al. (1996) European hake (Merluccius mer- P. Torres, pers. comm. luccius) Cetacea Gurnards: family Triglidae Á Guerra, pers. comm. Common dolphin (Delphinus del- González et al. (1994a), Silva phis) (1999a), De Pierrepont et al. (2005) Harbour porpoise (Phocoena Santos and Pierce (2003), Víkingsson phocoena) et al. (2003), Santos et al. (2004b), Jansen et al. (2013) 10.8 Other ecological aspects 10.8.1 Behaviour Sepiola atlantica may bury itself in the sand by day to hide from predators and as a technique for hunting. The burying behaviour in natural substrata in the aquarium was described by Rodrigues et al. (2010a). After a short period in an alert position, the animal starts burying itself, and on average the whole process taking 21.9 (± 4.93) s. Burial time does not appear to be related to size. Burying behaviour is accompanied by a display of colour changes peculiar to the species. In the laboratory, the entire body of newly hatched individuals is yellow and covered with expanded dark brown chromatophores. Individuals often assume a “flamboyant” arm display (as shown and described in Mauris, 1989, for Sepiola affinis). This posture consists of stretching the dorsal and latero-dorsal arms upwards perpendicular to the body axis, while the latero-ventral and ventral arms together are stretched downwards on each side of the body; all arm tips are rolled inwards. Cephalopod biology and fisheries in Europe: II. Species Accounts | 113 Hatchlings are generally less active during daylight and attempt to bury themselves in the sand immediately after hatching (see Rodrigues et al., 2011a). Although equipped with yolk reserves, they are ready to hunt mysid shrimp of equal size soon after hatching, and display a characteristic pattern of expanded dark brown chromatophores when focusing on prey. Prior to attacking prey, all chromatophores are contracted and, consequently, the animal turns virtually transparent. Arms are spread to form a circular crown, enabling the tentacles to be shot out rapidly (generally to the dorsal side, towards the middle of the mysid shrimp). If the attack is successful, tentacles are quickly retracted with the prey. When the tentacles are retracted (with or without prey), animals regain the dark brown colour (Rodrigues et al., 2011a). 10.9 Fisheries Bobtail squids Sepiola spp. are not usually identified in fishery landings (ICES, 2010). However, they are known to be landed and sold in fish markets in southern Europe (Reid and Jereb, 2005). 10.10 Aquaculture Although of no commercial value, S. atlantica is a potential species for experimental work under controlled conditions. For that reason, the University of Vigo and the Instituto de Investigaciones Marinas-CSIC are developing sepiolid culture techniques (Rodrigues et al., 2011d). 10.11 Future research, needs, and outlook Despite S. atlantica being a relatively common nearshore species, information on its biology, ecology, and life history was, until very recently, limited to waters around Scotland (e.g. Yau, 1994; Yau and Boyle, 1996). More recently, there has been research on the species in Wales (Jones and Richardson, 2010, 2012) and Galicia (Rodrigues et al., 2009, 2010a, b, c, 2011a, b, c, d, 2012). However, life cycle biology and ecology remain poorly known through most of its range, and more research is needed. 114 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Loligo vulgaris European squid Cephalopod biology and fisheries in Europe: II. Species Accounts 11 | 115 Loligo vulgaris Lamarck, 1798 Ana Moreno, Evgenia Lefkaditou, Jean-Paul Robin, João Pereira, Angel F. González, Sonia Seixas, Roger Villanueva, Graham J. Pierce, A. Louise Allcock, and Patrizia Jereb Common names Encornet (France), Καλαμάρι [calamary] (Greece), calamaro mediterraneo (Italy), lula vulgar (Portugal), calamar común (Spain), European squid (UK) (Figure 11.1). Synonyms There are no synonyms for Loligo vulgaris. 11.1 Geographic distribution The European squid, Loligo vulgaris Lamarck, 1798, is found in the Northeast Atlantic from ca. 55°N to ca. 20°S and throughout the Mediterranean (Jereb et al., 2010). It is one of the most common squids in the coastal waters of the Northeast Atlantic and the Mediterranean (Worms, 1983a). In the North Sea, its distribution extends from the northwest coast of Scotland, where it is occasionally reported (P. R. Boyle and G. J. Pierce, pers. comm.), to the Skagerrak and Kattegat, and a few old records from the western Baltic Sea (Grimpe, 1925; Tinbergen and Verwey, 1945) are supported by more recent information (Muus, 1959 in Hornbörg, 2005). A record of one specimen labelled Bergen (Norway; 60°23’N) is described in Grieg (1933). Figure 11.1. Loligo vulgaris. Dorsal view. From Muus (1959). Loligo vulgaris was not included by Massy (1928) in her list of the Cephalopoda of the Irish coast, and an early record of occurrence in the waters of the Isle of Man (Irish Sea; Moore, 1937, in Stephen, 1944) is doubtful. However, it is present in the central and southern North Sea (De Heij and Baayen, 2005; Oesterwind et al., 2010), where it appears mainly in late spring and summer. It is widely distributed in the English Channel, where, according to Royer et al. (2002), it is the second most abundant squid species (with slightly fewer recruits than Loligo forbesii), and it is occasionally caught in the Celtic Sea (Lordan et al., 2001a). Its distribution extends south along the west coasts of France, Spain, and Portugal (Guerra, 1992; Coelho et al., 1994; Moreno et al., 1994; Cunha et al., 1995). In the Bay of Biscay, trawl surveys in autumn showed that L. vulgaris is more abundant than L. forbesii in inshore and southern parts of the Bay (with catch rates of up to 150 specimens h–1; Denis, 2000). Along the west coast of Portugal, abundance decreases to the south (Cunha et al., 1995). Farther south along the west coast of Africa, it is found off Senegal and Angola (Baia dos Tigres; Adam, 1962), but, according to Augustyn and Grant (1988), it is never found south of 20°S. Loligo vulgaris is widely distributed throughout the Mediterranean Sea (Mangold and Boletzky, 1987; 116 | ICES Cooperative Research Report No. 325 Bello, 2004; Salman, 2009), including western and central Mediterranean waters (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Sánchez and Martin, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the whole Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak et al., 2008). The species has been recorded in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Figure 11.2. Loligo vulgaris. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 11.2 Taxonomy 11.2.1 Systematics Coleoidea – Decapodiformes – Myopsida – Loliginidae – Loligininae – Loligo. 11.2.2 Type locality Mediterranean Sea (exact position not known). 11.2.3 Type repository Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. Loligo vulgaris (Lamarck, 1798, Bulletin des Sciences, par la Société Philomatique, Paris, 2 (17): 130. Cephalopod biology and fisheries in Europe: II. Species Accounts 11.3 | 117 Diagnosis 11.3.1 Paralarvae The fins are paddle-shaped, broad, with short bases, each fin much wider than long. The mantle is broad, with a few large dorsal chromatophores and numerous ventral chromatophores. The head is squarish with a few chromatophores on the dorsal surface and 12 chromatophores on the ventral surface. Ten of these are arranged into two “cheek patches” of 5 chromatophores each, posterior to each eye; the remaining pair is located between the eyes. The ventral arms have 2 aboral chromatophores. There is a strong linear relationship between mantle length and eye diameter, which is, therefore, a useful parameter to estimate the size of damaged paralarvae in samples (González et al., 2010). The tentacles have 4 aboral chromatophores. The tentacular clubs are broad and much wider than the tentacular stalks. In the laboratory, size at hatching ranges between 2.92 and 3.85 mm ML (Turk et al., 1986), and individuals hatched in summer are slightly smaller than those hatched in winter (Villanueva, 2000a). The smallest hatchlings collected in the wild by González et al. (2010) measured 1.26 mm ML. 11.3.2 Juveniles and adults The mantle is muscular, cylindrical, moderately slender, and elongated posteriorly. Red chromatophores form abundant wide spots on the mantle, and a green/blue iridescence is apparent in the posterior part of the mantle in live or fresh specimens. The fins are rhomboid, their length exceeding 50% of the mantle length. There are 15 tiny suckers on the buccal membrane, each with a chitinous ring. The left ventral arm of males becomes hectocotylized, with suckers replaced by papillae along 15–33% of the whole arm length. The arms have two series of suckers. The sucker rings on the arms have ca. 20 teeth; on distal suckers, they are large and pointed and on proximal ones minute or even absent. The tentacles are not retractile. The tentacular clubs have four series of suckers in the “manus”; those in the central two series are markedly larger than the marginal ones. Sucker rings are illustrated in Figure 11.3. There are simple locking cartilages. The eyes have a cornea (Nesis, 1982/87; Guerra, 1992; Jereb and Roper, 2010). 11.4 Remarks Mature males and females can be distinguished by means of external characteristics. In mature males of L. vulgaris, as in L. forbesii, the white testis can be seen through the mantle in the dorsal region between the fins, and there may be evident hectocotylization. Mature females can be easily recognized by the Figure 11.3. Loligo vulgaris. Various tencolourful accessory nidamental glands seen in tacle sucker rings. Photos: Harry Palm the mid-region of the ventral side of the man- and Uwe Piatkowski. tle cavity. Females are also distinguished by the presence of the seminal receptacle, on the ventral buccal membrane, which appears as a small white spot when filled with sperm 118 | ICES Cooperative Research Report No. 325 (Ngoile, 1987). A detailed description of the reproductive system of L. vulgaris can be found in van Oordt (1938). 11.5 Life history Loligo vulgaris is an annual species with a maximum lifespan of ca. 15 months. Spawning is usually in winter in the northern and eastern portions of its geographic range and year-round with seasonal peaks elsewhere, although there is high spatiotemporal variability in reproductive and growth parameters. Paralarvae are planktonic for 2–3 months. 11.5.1 Egg and juvenile development Eggs are smaller than those of L. forbesii, slightly larger than those of Alloteuthis subulata (Mangold-Wirz, 1963a; Boletzky, 2003), and usually measure ca. 2.2 mm in length and 1.6 mm in width, although the size is variable, e.g. 1.82–2.66 mm × 1.51–1.99 mm in Portugal. In the Mediterranean, mature oocytes in the oviduct measure ca. 2.0 × 1.5 mm, and eggs in the egg mass, in stages I and II, measure 2.3 –2.7 mm long by 1.8–2.2 mm wide (Mangold-Wirz, 1963a). The eggs are generally deposited on a fixed support in relatively shallow water (20–50 m depth; Figure 11.4), and sometimes attached to floating objects in coastal waters (Worms, 1983a). Egg masses comprise multiple strings 60–160 mm long (MangoldWirz, 1963a), each string containing an average of 90 ovate eggs embedded in a thick gelatinous coat. Females tend to lay egg strings (30–60 eggs) over existing egg masses of the same species, so one egg mass can contain up to 40 000 eggs, although each female lays only from 3000 (small females) to 6000 (large females) eggs in total. Egg deposition apparently occurs throughout the distribution range. For example, egg masses are reported from waters of 15– 65 m in northern France and northwestern Spain and at 31–80 m off western and southern Portugal (Pereira et al., 1998). Villa et al. Figure 11.4. Loligo vulgaris. Egg mass attached to the gorgonian (1997) found eggs Paramuricea clavata, 40 m depth, Columbretes Islands, Mediterranean masses at depths as Sea. Photo: Jordi Chias. shallow as 2 m on the south coast of Portugal, although egg deposition in depths <15 m appeared to be restricted to the peak summer months of June–August, and most records were from depths of ≥20 m. The abundance of these egg masses peaked around the end of spring and beginning of summer, similar to the pattern of seasonal abundance of zooplankton. In the Adriatic, egg masses are regularly observed in early spring (March–April) at depths of 12–25 m Cephalopod biology and fisheries in Europe: II. Species Accounts | 119 (L. Ceriola, pers. comm.). In Morocco, egg masses are found throughout the year attached to hard substrata or branched sessile organisms, on sandy and rocky bottoms, usually at depths of 6–120 m (Baddyr, 1988). The duration of embryonic development is highly dependent on environmental conditions, e.g. temperature and oxygenation (Worms, 1983a). The final stages of development are characterized by a rapid increase in size, especially in length, while the outer yolk sac is rapidly reduced – partially by utilization of the nutritive material and partially by active transfer of the yolk mass to the inner yolk organ (Naef, 1928). Hatching occurs ca. 125 d after spawning at 13°C, 40–45 d at 12–14°C, 30 d at 17°C, and 26–27 d at 22°C (Mangold-Wirz, 1963a; Boletzky, 1979b). Rosa et al. (2012) showed that even a relatively small increase in temperature (2°C), consistent with projected ocean warming, promoted metabolic suppression, premature hatching, and a greater incidence of malformations in “newborn” hatchlings. However, hatchlings also showed some ability to compensate for adverse effects of elevated temperature. The authors state that “heat shock proteins (HSP70/HSC70) and antioxidant enzyme activities constituted an integrated stress response to ocean warming in hatchlings”. Inferences from the embryonic increment widths in statoliths of wild squid suggest that embryonic development typically takes place at temperatures of 12–17°C (Villanueva et al., 2003). Eggs of L. vulgaris spawned off the northwestern Iberian Peninsula were estimated to remain at sea, on average, one week longer than those deposited in the Mediterranean, reflecting the slightly higher water temperatures in the Mediterranean Sea. A longer incubation time for egg masses attached to the sea bottom probably increases the mortality risk. Conversely, slower development at lower temperature may improve yolk conversion, leading to larger hatchlings, and increased hatchling survival. In seawater with salinity values of 34–42 and at pH values of 7.8–8.4, L. vulgaris embryos develop and hatch normally. Beyond those ranges, embryos exhibit severe damage and may die. Concentrations of Ca2+, K+, Mg2+, and SO42- ions associated with normal development were: 9–15, 9–15, 46–70, and 15–37 mm, respectively (D'Aniello et al., 1989; Şen, 2005). Paulij et al. (1990b) studied the impact of photoperiodicity on hatching of L. vulgaris in the laboratory and observed that most embryos hatched soon after the light period ended. Embryos that had developed in constant light showed no such hatching rhythm. If those embryos were exposed to a dark shock, most hatched soon after the onset of darkness. A twilight shock, in which the light was reduced by 50%, did not stimulate hatching. Effects of photoperiod on embryo development were investigated by Şen (2004a). In natural seawater (37 psu, 20.3°C), a photoperiod of 12 h light and 12 h dark resulted in 100% hatching success, but with 24 h light, hatching success was only 52%. Embryos held under summer photoperiod conditions had slower statolith growth than those held at winter photoperiods, whereas constant light conditions produced significantly slower growth in the embryonic statoliths (Villanueva et al., 2007). 120 | ICES Cooperative Research Report No. 325 Total weight, mantle length, and statolith length of newly hatched paralarvae are greater for eggs incubated at lower temperature than for those incubated at higher temperature, as a result of the longer duration of the embryonic development at lower temperatures (Villanueva, 2000a, b). Figure 11.5. Loligo vulgaris. Hatchling (under anaesthesia, which may cause chromatophore contraction). Photo: Roger Villanueva. The paralarvae (Figure 11.5) have a planktonic life style that lasts 2–3 months depending on sea temperature (González et al., 2010; Moreno et al., 2012). Paralarvae are most abundant between the 50 and 125 m isobaths, particularly along the northwestern coast of Portugal (Moreno et al., 2009), where paralarvae up to 9.6 mm ML may be found in plankton samples (Moreno and Pereira, 1998). In Galician waters, paralarval abundance is greatest between May and October (González et al., 2005), later than in Portuguese waters, where paralarvae are found year-round, but abundance is greater in winter and early spring (Sousa Reis, 1989a; Moreno and Pereira, 1998; Moreno et al., 2009). Little is known about wild L. vulgaris paralarvae, mainly because of their similarity to young forms of the co-occurring species L. forbesii and Alloteuthis spp. (Sweeney et al., 1992). Relevant data from historical collections are compromised because long-preserved specimens lack visible chromatophores, which would otherwise aid species identification (Moreno and Sousa Reis, 1995). Paralarvae appear in low numbers in standard oblique ichthyoplankton and zooplankton hauls, suggesting that some alternative form of directed sampling is needed to study their distribution and seasonality (Moreno and Sousa Reis, 1995; Piatkowski, 1998). Observations in captivity show that, within 20 d of hatching, some squids are able to swim in a horizontal position for several minutes, maintain their position for more than 5 minutes against a current of 2.61 cm s–1 and swim several centimetres in pursuit of prey, i.e. in optimal conditions, it is likely that squid start schooling as well as displaying a neritic mode of life within 2 months of hatching (Turk et al., 1986). 11.5.2 Growth and lifespan Estimates based on length-frequency analysis suggest that L. vulgaris can live for up to 4 years (Mangold-Wirz, 1963a). However, counts of daily growth increments in statoliths reveal that lifespan is normally ca. 1 year, although variations have been reported, as detailed hereafter. Slightly longer lifespans (382 and 396 d) have been recorded in males from Galician waters (Rocha and Guerra, 1999) and the West Saharan shelf (Arkhipkin, 1995). Maximum lifespans of 15 months in both sexes were observed in northwestern Portuguese waters by Moreno et al. (2007). Note, however, that both Bettencourt et al. (1996) and Raya et al. (1999) estimated rather shorter lifespans: 9 months in southern Portuguese waters and 10 months on the western Saharan shelf, respectively; it is not clear whether this represents real biological variation or whether methodological issues are partly or wholly responsible. Male L. vulgaris attain greater length and weight than females. In the Northeast Atlantic, maximum mantle length is 546 mm in males (Moreno et al., 2007) and 372 mm in females (A. Moreno, pers. comm.). Larger specimens have been found off the west coast of Africa, males attaining 640 mm and females 485 mm ML (Perales Raya, 2001). Cephalopod biology and fisheries in Europe: II. Species Accounts | 121 The largest specimens in the Mediterranean Sea (males with an ML of 540 mm and females with 340 mm) were found in the western part (Worms, 1979). Male and female L. vulgaris have different length–weight relationships (Coelho et al., 1994; Guerra and Rocha, 1994; Moreno et al., 2002; Krstulović Šifner and Vrgoc, 2004; Table 11.1), the slope parameter b being significantly higher in females (2.38–2.81) than in males (2.20–2.59), corresponding to a greater weight at a given length in females. Comparisons of b values across geographic areas suggest a trend of increasing weight at length is (higher b) from north to south in the Atlantic and from the Atlantic to the eastern Mediterranean (Moreno et al., 2002). Growth studies of L. vulgaris paralarvae include both laboratory experiments and studies in the wild. Paralarvae have been cultured experimentally by Portman and Bidder (1928), Boletzky (1974, 1979b), Turk et al. (1986), and Villanueva (1994, 2000a), and all authors agree that early growth is clearly exponential. As in other squid species, paralarval growth rates are highly variable and strongly related to temperature. Reported average rates of growth in length in the first 75 d post-hatching were 0.05 mm d–1 (1.2% ML d–1) under winter temperatures and 0.17 mm d–1 (3% ML d–1) under summer conditions (Boletzky, 1979b; Villanueva, 2000b). The increase in weight during this period of life is more pronounced. Villanueva (2000b) measured instantaneous relative growth rates of 3–4% BW d–1 at winter temperatures (11°C) and 6–8% BW d–1 under summer conditions (19.2°C). As a result, 2 months after hatching, paralarvae reared under summer regimes attain a mean length twice that of winter squid and a mean weight fivefold higher. Nevertheless, there is always a great degree of individual variability in growth rates. In field-based studies using statolith analysis, G (instantaneous relative growth rate) in length (ML) ranged from 1.82 to 2.15% ML d –1 (González et al., 2010). Table 11.1. Loligo vulgaris. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference English Channel 0.192 2.38 F Moreno et al. (2002) 0.301 2.20 M 0.104 2.54 F Northwestern Spain Guerra and Rocha (1994) Northwestern Portugal Southern Portugal Sahara Bank Western Mediterranean Sea Adriatic Sea 0.164 2.37 M 0.104 2.54 F 0.154 2.41 M 0.135 2.43 F 0.144 2.38 M 0.109 2.56 F 0.118 2.47 M 0.187 2.30 F 0.121 2.50 M 0.197 2.45 F Moreno et al. (2002) Coehlo et al. (1994) Moreno et al. (2002) Sánchez (1986b) Krstulović Šifner and Vrgoč (2004) Greek Seas Izmir Bay (eastern Aegean) 0.138 2.44 M 0.065 2.81 F 0.078 2.59 M 0.1844 2.3066 All Moreno et al. (2002) Akyol and Metin (2001) 122 | ICES Cooperative Research Report No. 325 Iskenderun Bay (northeastern 0.0189 3.163 F 0.0182 3.2872 M 0.0019 4.0775 All Duysak et al. (2008) Levant Sea) Between the ages of 4 and 12 months, males generally grow at 1.2–1.6 mm d–1 and females slower at 0.9–1.0 mm d–1. Instantaneous growth rate relative to ML is 0.8–1.0% d–1 for males and 0.7–0.9% d–1 for females. Differences between male and female growth rates have been observed in most studies that adequately sampled the full size range of animals (Natsukari and Komine, 1992; Arkhipkin, 1995; Bettencourt et al., 1996; Raya et al., 1999; Rocha and Guerra, 1999; Moreno et al., 2007). Growth rate estimates in L. vulgaris reveal great individual variability in size-at-age, particularly, in males. Growth rates depend on hatching season and in particular on environmental conditions close to hatching, as proposed by Forsythe (1993). Loligo vulgaris hatched at warm temperatures have higher ML-at-age than specimens hatched at low temperatures (Rocha and Guerra, 1999; Moreno et al., 2007). Researchers agree that squid growth (in terms of length-at-age) does not conform to the generalized von Bertalanffy model (von Bertalanffy, 1938), often adopted to describe fish growth (Jackson, 1994). For juvenile and adult L. vulgaris, power, exponential or double exponential models generally provide the best fit to length-at-age data, depending on sex, hatching season, and geographic area (Natsukari and Komine, 1992; Arkhipkin, 1995; Bettencourt et al., 1996; Raya et al., 1999; Rocha and Guerra, 1999; Moreno et al., 2007). However, a logistic model best describes growth of females hatched in the warm season on the northwestern Portuguese shelf, with an inflection seen close to age at 50% maturity (agem50%) (Moreno et al., 2007). Perales Raya (2001) also observed such an inflection in female growth. Average growth curves calculated using equations presented in the above-mentioned studies are plotted in Figure 11.6. 700 420 360 300 0 240 0 180 100 120 100 60 200 0 200 Figure 11.6. Loligo vulgaris. Growth curves (length in mm vs. age in d), according to 1, Natsukari and Komine (1992); 2, Arkhipkin (1995); 3, Rocha and Guerra (1999); 4, Rocha and Guerra (1999) autumn-winter hatchers; 5, Bettencourt et al. (1996), spring-summer hatchers; 6, Raya et al. (1999); and 7,8, Moreno et al. (2007) cold and warm season hatchers. 420 300 360 300 400 300 400 500 240 500 1 2 3 4 5 6 7 8 600 60 600 Male growth curves 180 1 2 3 4 5 6 7 8 120 Female growth curves 0 700 Cephalopod biology and fisheries in Europe: II. Species Accounts 11.5.3 | 123 Maturation and reproduction The sex ratio is generally ca. 1:1 across the distribution range, although seasonal shifts in sex ratio have also been reported (Baddyr, 1988; Guerra and Rocha, 1994; Raya et al., 1999; Moreno et al., 2002; Krstulović Šifner and Vrgoč, 2004) as well as differences in sex ratio between size classes. Raya et al. (1999) found that the proportion of males was greatest in the smallest size classes, which is consistent with findings for L. forbesii. A wide range is observed in body size of mature animals of both sexes: 80–640 mm in males and 120–360 mm in females. Across its geographic distribution, L. vulgaris males mature at both a lower minimum size and a large maximum size than females. In the northwestern Mediterranean, there is a positive relationship between ovary weight and size at ML >14 cm, the size at which sexual maturation starts in females (Sánchez and Demestre, 2010). Based on examination of animals sampled at several sites in the Atlantic and Mediterranean, Moreno et al. (2002) calculated the size at which 50% of individuals are mature (MLm50%) as 168 mm in males and 188 mm in females. However, the fit for males is misleading, because two modes in size at maturity were detected in males from most areas in the Northeast Atlantic, the first at ca. 180 mm, and the second at 300–330 mm, at which size all males are mature (Coelho et al., 1994, Guerra and Rocha 1994, Moreno et al. 1994). Morphometric analysis of small and large mature males revealed no significant differences except in relation to size, suggesting that the two groups of males belong to the same population (Moreno et al., 1994). Two modes in size at maturity are not found in females. Given that two size-dependent reproductive strategies are known in males (guarding by large males and sneaking in by small males, see Hanlon and Messenger, 1996), it seems likely that natural selection favours the existence of two growth and maturation strategies, intermediate-sized animals being at a disadvantage. Size at maturity shows some degree of geographic variation in both sexes (Moreno et al., 2002; Smith et al., 2011). Size at maturity (MLm50%) of females appears to be higher in the southern part of the Northeast Atlantic (220–230 mm; Bettencourt, 1994; Raya et al., 1999) than in the north (176–195 mm; Guerra and Rocha, 1994; Moreno et al., 2005), and lower in the western and central Mediterranean (160–165 mm; Mangold-Wirz, 1963a; Krstulović Šifner and Vrgoč, 2004) relative to the Atlantic. Comparisons are more difficult for males, but there are no clear geographic trends in minimum size at maturity, which is ca. 120 mm in the English Channel (Moreno et al., 2002) and Galician waters (Guerra and Rocha, 1994), ca. 90–110 mm in southern Portuguese waters (Bettencourt, 1994), on the Saharan Bank (Raya et al., 1999), and in the Mediterranean (Mangold-Wirz, 1963a; Moreno et al., 2002; Krstulović Šifner and Vrgoč, 2004), but somewhat lower (80 mm) in northwestern Portuguese waters (Moreno et al., 2002). There is also seasonal variation in size at maturity across the distributional range (Moreno et al., 2002). Differences in size at maturity have also been observed between squid that had hatched at different times of the year (Boavida-Portugal et al., 2010). In northwestern Portuguese waters, females that hatched during the warm season were smaller at maturity (MLm50% = 156 mm) than those that hatched during the cold season (MLm50% = 191 mm). In males, two modes in size-at-maturity were present within both seasonal cohorts, indicating that the existence of two size modes is not due to the existence of different cohorts (Moreno et al., 2005). Age studies confirm that males mature ca. 1 month earlier than females (Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996; Moreno et al., 2005). In Portugal, males mature at a mean age of 9 months, and spawning takes place at a mean age of 10 months. A high percentage of the population is mature before 1 year (Moreno et al., 2005). Farther 124 | ICES Cooperative Research Report No. 325 south, on the Saharan Bank, minimum age at full maturity is 250 d in males (ca. 8 months) and 285 d in females (ca. 9.5 months) (Arkhipkin, 1995). Most studies suggest that small mature L. vulgaris are usually younger than large mature ones (Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996; Moreno et al., 2005), but some studies show that small and large mature animals can have similar ages (Perales Raya, 2001). Age at maturity is related to time of hatching; females hatched during the warm season have faster growth rates earlier in life and reach maturity at younger ages than those hatched in the cold season. Growth rates of the warm-water cohort animals decline after maturation, possibly related to less favourable environmental conditions. In contrast, females hatched during the cold season have slower initial growth rates, but their late maturation and the favourable environmental conditions they encounter later result in increased growth rates towards the end of their life cycle (Moreno et al., 2005, 2007). The influence of hatching time on age at maturity is more pronounced than its influence on size at maturity (Moreno et al., 2005). Individual maturity in sampled animals is often described using a five-point scale, modified from Lipiński (1979) by Boyle and Ngoile (1993a). Sex has been identified macroscopically in squid from 4 months of age (Arkhipkin, 1995; Moreno et al., 2005), and the beginning of gonad maturation (maturity stage 2) has been observed from ca. 5 months in males and 6 months in females (Moreno et al., 2005). The process of maturation is fast. In Portuguese waters, from the beginning of visible maturation, specimens of both sexes can become fully mature in less than 1 month (Moreno et al., 2005). Variability in the rate of maturation is high, with standard deviations of 1–1.5 months from the mean age at each maturity stage. Large immature males frequently appear in samples, suggesting that growth and maturation can become uncoupled. There is considerably greater reproductive investment in terms of gonads, genital tract, and glands in females than in males. The gonadosomatic index (GSI) in males is between 1.6 and 3.8% compared with up to 30% in females (Worms, 1983a). Gonad weight is better correlated with size than with age in both sexes (Moreno et al., 2005; Sánchez and Demestre, 2010). Geographic and seasonal variation is found in GSI. GSI is lowest in the Western Sahara, where L. vulgaris attain the largest sizes (Moreno et al., 2002). Females hatched under warmer temperatures that achieve earlier maturation also have a higher GSI (i.e. they invest a greater proportion of their total mass in reproduction) than females hatched during the cold season, which mature later in life. There are marked differences in GSI between 7-month-old individuals of these two hatching groups (Moreno et al., 2005). Males seize females by the head during copulation. Spermatophores are passed to the female through the penis with the aid of the hectocotylized arm (Ngoile, 1987) and placed in the female’s buccal membrane and into a spermatheca while in a head-tohead position (Mangold-Wirz, 1963a). Mating may take place prior to arrival as well as at the spawning grounds. Eggs are fertilized by sperm from the spermatheca. The nidamental and oviducal glands secrete a mucus that coats eggs and forms egg strings 60–160 mm long (Worms, 1983a). Females lay egg strings close to other egg masses, visual and/or chemical stimuli probably being involved (Mangold-Wirz, 1963a). Loligo vulgaris is clearly semelparous because the ovaries show no evidence of regression and regrowth between spawning bouts (Mangold, 1987). However, the process of Cephalopod biology and fisheries in Europe: II. Species Accounts | 125 oogenesis involves “partial ovulation” (Rocha and Guerra, 1996), i.e. the development of oocytes is asynchronous, and mature ovaries have polymodal distributions of oocytes (3–5 modal groups), suggesting that egg-laying takes place in several batches during the spawning period. Rocha and Guerra (1996) applied the term “intermittent terminal spawning” to describe this strategy (see also Rocha et al., 2001). When fully mature, the oviduct of the female is filled with ripe eggs. Spawning has rarely been seen in the laboratory (Mladineo et al., 2003). Small protoplasmic oocytes, <0.4 mm in diameter, dominate throughout the reproductive cycle (Rocha and Guerra, 1996; Laptikhovsky, 2000), as in other loliginid species (Sauer and Lipiński, 1990; Collins et al., 1995a). As there is continuous oocyte maturation, several types of oocyte are found in the mature ovary at various stages of development and differing in appearance and size. The smallest, completely immature oocytes, measure 0.17–0.68 mm in diameter. Larger, but still immature, oocytes measure 0.86–1.65 mm, and maturing oocytes with a characteristic reticulated surface measure 1.55–2.45 mm. The largest, fully mature oocytes have a smooth surface. These large eggs show some geographic variation in size, with greater mean size recorded in Galician waters and in the western and central Mediterranean (2.3–2.8 mm; MangoldWirz, 1963a; Guerra and Rocha, 1994; Krstulović Šifner and Vrgoc, 2004), intermediate size in southern Portuguese waters (2.2 mm; Coelho et al., 1994), and low mean size along the northwest coast of Africa (1.9 mm; Laptikhovsky, 2000) and northwestern Portugal (1.1–1.2 mm; Boavida-Portugal et al., 2010). Worms (1983a) estimated maximum fecundity as 7000 eggs, but this value was based on counting only ripe eggs in the oviduct. Other studies that consider the yolk oocyte stock in the ovary and oviduct have estimated maximum fecundity to be between 10 150 and 42 000 eggs (Baddyr, 1988; Coelho et al., 1994; Guerra and Rocha, 1994; Lopes et al., 1997; Laptikhovsky, 2000). This may still be an underestimate if the protoplasmic oocytes also contribute to the total fecundity of an individual. On that basis, Laptikhovsky (2000) estimated a potential fecundity of 28 500–74 200 eggs, with higher values generally in larger squid (fitted regression: potential fecundity = 136.84 ML 1.11). However, the correlation between the number of oocytes and the ML is generally weak, and other studies show that small mature females may have more oocytes than females that mature at a larger size (Guerra and Rocha, 1994; Krstulović Šifner and Vrgoč, 2004). Spermatophore formation in mature males appears to be continuous. The maximum number of spermatophores is slightly over 1000, and their length varies between 7.5 and 20 mm. Larger animals have larger spermatophores, although the number of spermatophores is not related to mantle length (Mangold-Wirz, 1963a; Guerra and Rocha, 1994; Krstulović Šifner and Vrgoč, 2004). Loligo vulgaris has an extended seasonal spawning season in most regions, although geographic variation is also evident. The spawning period is seasonally restricted in the North Sea (Tinbergen and Verwey, 1945), in the English Channel (Moreno et al., 2002), and in the central (Krstulović Šifner and Vrgoč, 2004) and eastern Mediterranean (Moreno et al., 2002). Spawning throughout the year has been reported farther south in the Atlantic, from the northwestern Spanish coast to Western Sahara (Baddyr, 1988; Coelho et al., 1994; Guerra and Rocha, 1994; Moreno et al., 1994, 2002; Rocha, 1994; Bettencourt et al., 1996; Villa et al., 1997; Raya et al., 1999; Vila et al., 2010), and in the western Mediterranean (Worms, 1983a). In some areas where spawning is year-round, two peaks are observed. The timing of peak spawning also shows geographic variation and is earlier south than north in Atlantic waters and earlier in all Atlantic areas than in the Mediterranean. 126 | ICES Cooperative Research Report No. 325 Spawning takes place between November and April (peaking in February) in the English Channel, mostly during the same period along the northwestern Spanish coast, and throughout the year, with peaks in late autumn/early winter and late spring, in Portuguese waters and the Saharan Bank. In the Adriatic Sea, spawning is mainly between January and May (peaking in April–May), and in Greek seas, between November and May (peaking in April). 11.6 Biological distribution 11.6.1 Habitat Loligo vulgaris paralarvae are reported in plankton samples from off Galicia and Portugal (Moreno and Pereira, 1998; Piatkowski, 1998; González et al., 2005) and as far south as 21°N along the northwestern African coast (Guerra et al., 1985). Loligo sp. paralarvae (some possibly of L. vulgaris) are recorded in plankton samples from the English Channel (Collins et al., 2002). Loligo vulgaris paralarvae were absent from plankton samples collected in neritic waters around Scotland, the northwestern North Sea, and the Rockall Trough area (Yau, 1994), but they have been reported from the eastern Mediterranean (Salman, 2012). In Portuguese waters, paralarvae are most abundant over depths of 80–90 m (Moreno et al., 2009). In winter, their distribution extends offshore, but in summer and autumn, they concentrate closer inshore (Moreno and Sousa Reis, 1995; Moreno et al., 2009). Paralarvae are transported to the inner parts of the rías during upwelling events, which favours their coastal retention (González et al., 2005). The distribution of paralarvae is limited to areas with surface water temperatures of 13–20°C (Moreno and Sousa Reis, 1995; Moreno et al., 2009), and abundance is greater near the cold limit of the range, at 13–14°C (Rocha et al., 1999; Moreno et al., 2009). Loligo vulgaris is neither pelagic nor fully benthic; it is more or less restricted to the sea bottom during the spawning season, but displays pelagic behaviour at other times, e.g. when hunting (Worms, 1983a). It can be described as nektobenthic and neritic; it is usually more abundant in water shallower than 100 m (Sánchez and Guerra, 1994; Salman et al., 1997; Sánchez et al., 1998a; Tserpes et al., 1999), but is found from the coast to the limits of the upper slope (200–550 m). Where the shelf is narrow, the range at which L. vulgaris is caught extends into deeper water, as in Algerian waters (MangoldWirz, 1963a), and the Ionian Sea (Lefkaditou et al., 2001). Off the Portuguese coast, L. vulgaris can be found from the coast to water 100 m deep (Cunha et al., 1995), with spawning females concentrating where the depth is 80–100 m (Moreno, 1998). In the Gulf of Cádiz, it is mainly distributed between depths of 15 and 100 m (Vila et al., 2010). In the Mediterranean, it lives in the circumlittoral area and shelf, mainly at depths of 10–150 m, although off the Algerian shelf, it has been captured as deep as 550 m; it is most common at 50–60 m (Mangold-Wirz, 1963a; Worms, 1983a). Studies on demersal species assemblages, based on trawl surveys, have shown that in areas with extended continental shelves, such as the northern Tyrrhenian Sea, L. vulgaris is more abundant at depths <50 m, associated with other coastal species such as Sepia officinalis and Octopus vulgaris (Sánchez et al., 1998a). In other areas, it is associated with species with a wider bathymetric distribution on the continental shelf, such as Eledone moschata, Alloteuthis spp., Diplodus annularis, Pagellus erythrinus, Dentex spp., Seranus cabrila, Spicara flexuosa, Spicara smaris, Boops boops, Citharus linguatula, Mullus barbatus, Trachinus spp., and Pagrus pagrus. Depth influences the composition of assemblages associated with L. vulgaris more than any other factor (Pereira et al., 1997). Cephalopod biology and fisheries in Europe: II. Species Accounts | 127 Generally, L. vulgaris inhabits temperate waters, with juveniles and adults in water with temperatures ranging from 12.5 to 20°C. Abundance is, however, greatest in water with sea surface temperatures between 13 and 15°C. The animals require a relatively high temperature for reproduction, and their migration to the spawning grounds is later in years when coastal waters take longer to warm or warm later (Mangold-Wirz, 1963a). In Portuguese waters, the distribution of the species is clearly associated with bottom water temperature (Pereira et al., 1998). It tends to concentrate in the north in autumn, closer to the offshore limits of its distribution, and in the south in summer, close inshore, where summer bottom temperatures are warmer. Juveniles and adults can live in waters with rather low salinities, although they do not usually enter estuaries or lagoons (Mangold-Wirz, 1963a). Indeed, the species is found in very shallow water only when the salinity rises above 30, suggesting a tolerance range of 30–36 in the North Atlantic (Tinbergen and Verwey, 1945), with a slightly higher upper limit in the Mediterranean (37.7–38.15) (Salat et al., 1978). However, in the Sea of Marmara, Ünsal et al. (1999) recorded L. vulgaris in waters where the salinity was always >25. Laboratory experiments have shown that eggs die very early below a salinity of 24 (Şen, 2004b). The suitability of substratum for egg-string attachment seems to be the main reason for association of L. vulgaris with particular bottom types, although some prey species, e.g. sandeels, may also be associated with particular substrata. In the Atlantic, L. vulgaris is most abundant over coarse sand bottoms and scarce over silt bottoms. In Portuguese waters, its bathymetric distribution seems to be related to the offshore limit of occurrence of sandy bottoms (Pereira et al., 1995). However, in the Mediterranean, it is reported over all bottom sediment types, although mainly over coastal silt in spring and summer and over offshore sandy bottoms in autumn and winter (Mangold-Wirz, 1963a; Worms, 1983a). In the Adriatic, it may also be found over bottoms covered by sea grasses (Zostera and Posidonia beds), especially in autumn (Gamulin-Brida and Ilijanić, 1972). Recruitment and spawning are known throughout the geographic range of the species. Investigations on spawning grounds along the south coast of Portugal have shown that the greatest number of egg-mass records coincides with the highest values of zooplankton abundance (Villa et al., 1997). Sexual segregation has not been observed in the Northeast Atlantic population (Guerra, 1992), although Worms (1983a) found that landings by boat in the western Mediterranean indicate an interesting segregation by sex (80–90% of one sex), suggesting that males and females gather in different schools. 11.6.2 Migrations Horizontal migratory movements by L. vulgaris are mainly related to sexual maturation and spawning (Worms, 1983b). Onshore and offshore migrations, related to reproduction, are well-described for Mediterranean populations. Large (maturing or mature) animals move towards shallow coastal waters for mating and spawning; some squid mate during this migration. Some immature animals also perform this offshore/onshore migration, but some time after the mature individuals. These crossed migrations result in a complex population structure. Males arrive at the spawning grounds some days before females. Large mature animals spawn first and then leave littoral waters. This results in a progressive decrease in the mean size of squid in fishery catches over the spawning season (Mangold-Wirz, 1963a). Irrespective of size, a large proportion of the individuals (mainly females) die a few days or weeks after spawning (Worms, 128 | ICES Cooperative Research Report No. 325 1983a). Small squids hatched near the coast migrate towards deep water, mostly in autumn and winter (Sánchez and Guerra, 1994). In the Atlantic, L. vulgaris migrates long distances (south–north and north–south), possibly up to 500 km. According to Tinbergen and Verwey (1945), it actively migrates north in spring, probably entering the North Sea from the English Channel and migrating along the Belgian, Dutch, northwestern German, and Danish coasts, where it is found in late summer. Seasonal variation in fishery catches also suggests the existence of seasonal migrations in the Iberian Peninsula and Bay of Biscay (Moreno et al., 2002). In Portuguese waters, an indication of horizontal migration is the occurrence of late winter/early spring recruitment peaks locally unmatched by previous spawning peaks. A late summer spawning peak on the south coast of Portugal, reported by Bettencourt et al. (1996), could result in a recruitment peak along the northwest coast after juvenile migration (Moreno et al., 2002). In some areas, such as in the coastal waters of the Thracian Sea, inshore–offshore movements appear to be temperature-driven, with temperature significantly affecting beach-seine catches of L. vulgaris (Lefkaditou et al., 1998b). Feeding is the main reason for daily vertical migration to the surface at night. Loligo vulgaris paralarvae perform diel vertical migrations, arriving near the surface some time after sunset and remaining in the surface layers at least until midnight (Sousa Reis, 1989b). Differences in catches between day and night suggest that post-recruit L. vulgaris live close to the seabed by day and disperse vertically into the water column at night (Roper and Young, 1975), where they can be seen near the surface. Juveniles also undertake diel vertical migration, although mature adults tend to remain close to the bottom (Mangold-Wirz, 1963a). Feeding at night is supported by recent tagging experiments on L. vulgaris; tagged squid moved within a small area during the day, but covered a larger area from sunset to sunrise (Cabanellas-Reboredo et al., 2012a). 11.7 Trophic ecology 11.7.1 Prey Loligo vulgaris is an active cephalopod characterized by a fast growth rate and digestion (Bidder, 1950), suggesting that prey abundance could be a decisive factor influencing species distribution. However, the wide spectrum of its prey composition does not limit it to a specific biotope, except in the early stages, when a more restricted range of pelagic prey of small size is needed. Hatchlings can feed exclusively on the inner yolk sac, but the digestive tract is fully functional even before the complete reabsorption of yolk (Worms, 1983a). Juvenile and adult L. vulgaris are carnivorous predators, attacking, seizing, and eating relatively large active prey. Prey sizes estimated from stomach content remains are smaller than squid sizes (Rocha et al., 1994). Juvenile squid consume more planktonic than benthopelagic prey, particularly planktonic crustaceans such as copepods, mysids, and euphausids, but also fish larvae (Nigmatullin, 1975; Boletzky, 1979b; Worms, 1983a), indicating an ontogenetic shift in the species’ diet. Laboratory rearing revealed that decapod crab zoeae and mysids were the easiest food for young squids to capture (Boletzky, 1979b; Villanueva, 1994). Palaemonetes larvae (shrimp) were easily captured and appeared to be the preferred food species of paralarvae, whereas fish larvae were the preferred food of juveniles (Turk et al., 1986). Observations in captivity also suggest that, although paralarvae will attack conspecifics, they never display cannibalism (Boletzky, 1979b). Cephalopod biology and fisheries in Europe: II. Species Accounts | 129 Fish are the most common prey of adult L. vulgaris, their incidence increasing in the diet with increasing squid size (Rocha et al., 1994; E. Lefkaditou, pers. comm.). Cephalopods and crustaceans are of lesser importance in the diet, although there is evidence of regional differences (Guerra and Rocha, 1994; Hasan et al., 1994; Pierce et al., 1994a). Remains of polychaetes have also been found in the stomach contents of L. vulgaris from the Iberian Atlantic coast. Despite the difficulties associated with identification of squid prey to species level, which (to date) has generally been possible only when otoliths, beaks, or other hard parts are found among food remains, a broad spectrum of species has been recorded in the diet of L. vulgaris in several regions (Table 11.2; see also Pierce et al., 1994a; Rocha et al., 1994; Coelho et al.1997). Diet and food intake varies with season, most probably related to a combination of seasonal changes in prey abundance, in fishing grounds, and hence in sample source (Pierce et al., 1994a; Rocha et al., 1994). In northwestern Spain during late spring, summer, and early autumn when L. vulgaris are fished inshore by jigging, the frequency of cephalopods, crustaceans, and polychaetes in the diet increases relative to the rest of the year, when the squid are caught offshore by trawling. Cannibalism does not seem to play an important role in the species’ trophic ecology, because remains of L. vulgaris have been rarely reported in stomach contents. No differences in feeding habit have been observed between sexes, and females do not decrease food intake during maturation (Worms, 1983a; Rocha et al., 1994). Simulation in captivity of injuries caused by jigging (loss of one or both tentacles) showed that squid missing tentacles are less able to catch fast-swimming prey (e.g. fish), but can compensate by changing their diet and predation behaviour (CabanellasReboredo et al., 2011). Table 11.2. Prey composition of Loligo vulgaris, as known from studies in different regions of the Northeast Atlantic, Saharan Bank, and northern Aegean Sea (compiled from Guerra and Rocha, 19941; Pierce et al., 1994a2; Coelho et al., 19973; Lefkaditou, 20064). Taxon Species Osteichthyes Ammodytidae Ammodytes tobianus (small sandeel)1, Gymnammodytes semisquamatus (smooth sandeel)1, Hyperoplus lanceolatus (greater sandeel)1, indet.1,2 Argentinidae Argentina sphyraena (Argentine)1, Argentina spp.4 Atherinidae Atherina presbyter (sand smelt)1,2, Atherina spp.1,3 Blenniidae Blennius ocellaris (butterfly blenny)1, Blennius spp.1 Callionymidae Callionymus reticulatus (reticulated dragonet)1, Callionymus spp.1,2, indet.3 Carangidae Trachurus trachurus (Atlantic horse mackerel)1,3, Trachurus spp.2, indet.3 Cepolidae Cepola macrophthalma (red bandfish)1 Clupeidae Clupea harengus (Atlantic herring)2, Sardina pilchardus (European pilchard)3, Sprattus sprattus (European sprat)1, indet.1,2 Engraulidae Engraulis encrasicolus (European anchovy)3 Gadidae Gadiculus argenteus (silvery pout)1,2,4, Micromesistius poutassou (blue whiting)1,2, indet.1,2 130 | ICES Cooperative Research Report No. 325 Gobiidae Aphia minuta (transparent goby)1, Gobiusculus flavescens (twospotted goby)1, indet.1,2,3,4 Hemiramphidae indet.3 Lotidae Gaidropsarus spp.4 Myctophidae Diaphus dumerilii3, indet.3 Percidae Gymnocephalus cernuus (ruffe)3 Pleuronectidae indet.3 Scombridae Scomber scombrus (Atlantic mackerel)3 Sebastidae Helicolenus dactylopterus (blackbelly rosefish)2 Soleidae Microchirus boscanion (Lusitanian sole)3, Microchirus spp.3 Sparidae indet.2,3,4 Sternoptychidae Maurolicus muelleri (pearlside)2, Triglidae Chelidonichthys spp.3 indet.1,2 Crustacea Decapoda indet.3 Dendrobranchiata- indet.1 Penaeiodea Pleocyemata- Portunidae indet.1 Brachyura Euphausiacea indet.3 Mysida indet.1 Amphipoda Gammaridae indet.3 Isopoda indet.3 Cephalopoda Myopsida Alloteuthis media4, A. subulata2, Loligo forbesii2, L. vulgaris3, Loliginidae indet.3 Oegopsida Cranchiidae indet.3 Sepioidea Rondeletiola minor1, Sepia elegans3, Sepia spp.3, Sepietta spp.1, Sepiolidae4, indet.2 Octopoda Octopus spp.3 Gastropoda Turitella spp.1 Bivalvia indet.1 Polychaeta indet.1,2,3 Phyllodocida Hediste diversicolor (as Nereis diversicolor)1, Nephtys spp.3, Nereis spp.3, Perinereis spp.3 11.7.2 Predators Identification of long-finned squids in the stomach contents of numerous predator species in European seas remains at the level of the family Loliginidae (although it should be possible to distinguish beaks of Alloteuthis spp. from beaks of Loligo spp.). Nonetheless, L. vulgaris has been identified in the stomach contents of several large pelagic and demersal fish as well as marine mammals (Table 11.3). Table 11.3. Known predators of Loligo vulgaris in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopoda Common octopus (Octopus vul- | 131 Quetglas et al. (1998a) garis) Chondrich- Blainville's dogfish (Squalus blainville) Martinho et al. (2012) Blackspotted smooth-hound (Mus- Jardas et al. (2007) thyes telus punctulatus) Blonde ray (Raja brachyura) Farias et al. (2006) Bull ray (Pteromylaeus bovinus) Capapé (1977) Eagle ray (Myliobatis aquila) Jardas et al. (2004) Lesser spotted dogfish (Scyliorhinus Martinho et al. (2012) canicula) Marbled electric ray (Torpedo mar- Capapé et al. (2007) morata) Pelagic stingray (Pteroplatytrygon vi- Lipej et al. (2013) olacea) Smooth-hound (Mustelus mustelus) Morte et al. (1997), Kabasakal (2002) Thornback ray (Raja clavata) Kabasakal (2002), Farias et al. (2006) Osteichthyes Torpedo ray (Torpedo spp.) Abdel-Aziz (1994) Atlantic bluefin tuna (Thunnus Battaglia et al. (2013) thynnus) Atlantic stargazer (Uranoscopus sca- Sanz (1985) ber) Common two-banded seabream Rosecchi (1987) (Diplodus vulgaris) Greater amberjack (Seriola dumerili) Matallanas et al. (1995) Lesser weever (Echiichthys vipera) Creutzberg and Duinevald (1986) Spotted flounder (Citharus linguat- Teixeira et al. (2010) ula) Swordfish (Xiphias gladius) Hernández-García (1995), Salman (2004), Peristeraki et al. (2005) Pinnipedia Mediterranean monk seal (Mona- Guclusoy (2008) chus monachus) Cetacea Harbour porpoise (Phocoena pho- Börjesson et al. (2003) coena) Bottlenose dolphin (Tursiops trunca- San Miguel (1977), Orsi Relini et al. tus) (1994), Blanco et al. (2001), Santos et al. (2007) Common dolphin (Delphinus del- González et al. (1994a), Santos et phis) al. (2013) Long-finned pilot whale (Globiceph- González et al. (1994a), Santos et alus melas) al. (2014] Risso's dolphin (Grampus griseus) González et al. (1994a), Bearzi et al. (2011) 132 | 11.8 ICES Cooperative Research Report No. 325 Other ecological aspects 11.8.1 Parasites The copepod Pennella varians has been found on the gills, and various species of helminths in the stomach, intestine, and digestive tube of L. vulgaris (Dollfus, 1958; González et al., 2003). Zuev and Nesis (1971) recorded a range of parasites in L. vulgaris: the cestodes Scyphophyllidium pruvoti and Phyllobothrium loliginis, the trematode Isancistrum loliginis, and the nematode Filaria loliginis. The polychaete Capitella hermaphrodita lives in the external envelopes of the egg capsules, eating them, but not attacking the eggs. 11.8.2 Contaminants Heavy metal accumulation from seawater in the embryos of L. vulgaris seems to be lower than recorded in Octopus, probably because of the presence of a mucilaginous envelope in the squid egg mass, but seems to be higher than in cuttlefish, because of the good protection provided by the Sepia egg shell (Lacoue-Labarthe et al., 2011a). Increasing seawater pCO2 (ocean acidification) enhanced the uptake of both silver and zinc, and led to reduced uptake of cadmium and mangansese in L. vulgaris embryos (Lacoue-Labarthe et al., 2011b). A recent study indicated that methyl mercury levels in L. vulgaris from Portuguese waters have had no adverse implications for human health, although maximum consumption levels were suggested for octopuses and cuttlefish, and the authors expressed concern that other metals accumulated by cephalopods, e.g. cadmium, may pose a greater threat to consumers (Cardoso et al., 2012). 11.9 Fisheries The main recruitment areas along Atlantic coasts are located in the south, from Galician through Portuguese waters, where recruits are found throughout the year (Pereira et al., 1998). In the remaining areas of the distribution range to the north, recruits are present in high proportions only in the main recruitment seasons. In the Northeast Atlantic, there are one or more seasonal peaks in recruitment, males usually recruiting earlier to the fishery (Boyle and Pierce, 1994). Along the Portuguese coast and on the Saharan Bank, the recruitment periods can be longer (Moreno et al., 2002). In northwestern Portugal, recruitment to the fisheries starts at ca. 5 months of age and at mantle lengths from 60 mm (Moreno et al., 1996). Recruitment takes place in water 20–50 m deep (Moreno, 1998). On the Saharan Bank, the main recruitment season extends from June to September, but with secondary recruitment peaks in some years in November–December (Raya et al., 1999). In the western Mediterranean, the main recruitment season is in late summer (Lloret and Lleonart, 2002), and in the Catalan Sea, the minimum size at recruitment is ca. 40 mm (Mangold-Wirz, 1963a). In the Thracian Sea, recruits of 5–12 cm ML appear on inshore fishing grounds in May, whereas maturing large individuals migrate inshore in autumn (Anon., 2000). In the Atlantic and Mediterranean, L. vulgaris is mainly a bycatch of the multispecies bottom and pelagic trawl fisheries and is landed throughout the year. It is a secondary target species in the Saharan Bank cephalopod trawl fishery (Raya et al., 1999), and is usually landed mixed with L. forbesii (the two species are usually not separated in official statistics). There are also directed small-scale coastal fisheries, based on hand-jigging, beach-seining, and other artisanal gears, as well as gillnets and trammelnets, especially in Spain and Portugal, which target the animals when they enter coastal waters in autumn and winter to spawn (Guerra et al., 1994; Simon et al., 1996; Lefkaditou et al., 1998b). Cephalopod biology and fisheries in Europe: II. Species Accounts | 133 In the Northeast Atlantic, L. vulgaris is probably the main component of long-finned squid landings, which have fluctuated from ca. 7000 to 12 500 t annually over the past decade, peaking in 2003 and being lowest in 2008 (ICES, 2012). (A lower total in 2009 was excluded since France did not report its landings in 2009). The FAO Fishstat database (FAO, 2011) shows landings of “common squids nei” in the Northeast Atlantic varying from 1700 to 5700 t annually in the decade up to 2010. However, it is likely that much of the common squid landed found its way into the “various squids nei” category (which peaked at ca. 13 500 t in 2004). In the Mediterranean, FAO landings statistics for “common squids nei” ranged from ca. 4000 to 6000 t in the decade up to 2010. Although the category “European squid” exists in the FAO database, a maximum of only 22 t (in 2010) was assigned to this species in Mediterranean landings, and no landings from the Northeast Atlantic were assigned to the category. At a local level, better quality statistics are sometimes available for landings of L. vulgaris. In the coastal rías of southern Galicia (northwestern Spain), squid are targeted during the months July–September using a boliche (boat-seine). According to a study carried out during 1999–2003, L. vulgaris is the primary target and makes up 46% of catches by weight. More than 90 other species are recorded in the catches, but a substantial proportion (mainly undersized fish) are discarded (Unidad Técnica de Pesca de Bajura; Tasende et al., 2005). The species is also taken using boliche in Malaga (Mediterranean coast of Spain) (Anon., 1981). Information available on discarding practices has improved since implementation of the EU’s Data Collection Framework (ICES, 2012). Loligo vulgaris is frequently discarded by the Spanish fisheries in western Irish waters and on Rockall Bank (12–92% of Loligo spp. discards), but the percentage of discards from northern Iberian waters and the Gulf of Cádiz is close to zero (Santos et al., 2012). Borges et al. (2001) recorded L. vulgaris among the species frequently discarded in southern Portugal. However, recent data indicate that the discard rate of L. vulgaris by Portuguese trawl fleets in ICES Subarea IXa is very low (0–6%) (Prista et al., 2012). The percentage of discards of Loligo spp. by the UK fleets in the English Channel is also very low (0–4%). On the other hand, long-finned squids seem to be 100% discarded by the German and Netherlands trawl fleets (ICES, 2012). No information is officially available for the Mediterranean Sea, where long-finned squids have never been reported as discarded (P. Jereb, pers. comm.). There is no discarding of L. vulgaris in the southern Adriatic, where even new recruits are landed for local consumption (L. Ceriola, pers. comm.). Variation in catches and catch rates in squid is often attributed to environmental factors; to a large extent, such variations can be explained by environmental effects on abundance and on the seasonality of the life cycle. However, there may also be environmental effects on behaviour and activity that affect catch rates. Hence, CabanellasReboredo et al. (2012b) observed that catch rates of L. vulgaris in the recreational jig fishery in the Balearic Islands were maximized by low sea surface temperature, low wind speed, low atmospheric pressure, and days close to the new moon. Catches were best around sunset, when the sunlight is still sufficient to allow recreational fishing lures to be effective, and the squid have already shifted to a more active pattern of movement characteristic of night-time. Accounts of fishing for L. vulgaris in European waters in the early 1990s are given by Cunha and Moreno (1994), Guerra et al. (1994), and Shaw (1994). Balguerias et al. (2000) describe the origins of the Saharan Bank cephalopod fishery, of which L. vulgaris is a (minor) component; for many years, until termination of Spain’s agreement with Mauritania, Spanish vessels took a significant proportion of the cephalopod catches from that region. 134 | ICES Cooperative Research Report No. 325 Initial molecular genetic studies based on mitochondrial DNA have suggested that L. vulgaris is genetically rather homogeneous across the Northeast Atlantic (ICES Area), relative to other cephalopod species such as Sepia officinalis and Octopus vulgaris (ICES, 2004). This conclusion is consistent with earlier studies based on multivariate analysis of morphometric data and isozyme electrophoresis, which also showed no significant population or subpopulation differences. A study by Garoia et al. (2004) using microsatellites suggested a single population within the Adriatic Sea. However, the same study showed that eastern and western Mediterranean samples were consistently different from Atlantic samples, and from each other. The Western Sahara samples were the most different among the Atlantic samples. As with all European cephalopods, there is no regular stock assessment for L. vulgaris, and management is largely limited to landing-size regulations in southern Europe. The applicability of assessment methods for these stocks is limited by inadequate and inaccurate statistical information and because most catches are made as bycatch in finfish fisheries (Boyle and Pierce, 1994). However, a small number of stock assessment exercises have been carried out in Europe. For the English Channel, Royer et al. (2002) estimated natural mortality (M) empirically using Caddy's method (Caddy, 1996) assuming an annual life cycle (as in L. forbesii) and a mean fecundity of 15 000 eggs. This gave a monthly M rate of 0.2. They then applied depletion methods and monthly cohort analysis, which showed that recruitment was highly variable (range 2.4–14 million in the 1993–1996 year classes). Exploitation diagnostics indicated that juvenile L. vulgaris can undergo high fishing mortality when L. forbesii recruitment is low. For both species fished in the English Channel, exploitation levels were above the optimum, but L. vulgaris was more consistently overexploited. Application of depletion models to catchper-unit-effort data from trawls and beach-seines in the Thracian Sea (northeastern Mediterranean, Greece) showed no notable effect of the fisheries on squid population size (Tsangridis et al., 1998). The existence of relationships between recruitment strength and environmental conditions experienced by juveniles or spawners of the previous generation suggests that fishery forecasting is feasible, however. In the northwestern Mediterranean, cooler weather conditions in May are apparently associated with better landings of L. vulgaris in autumn (Sánchez et al., 2008). 11.10 Future research, needs, and outlook Loligo vulgaris is one of the most economically important myopsid squid species, given its commercial value in areas such as the French and Iberian coasts, the Saharan Bank, and the Mediterranean. It has also been a target of research for many years and is therefore one of the best-known European cephalopod species. Difficulties inherent in describing and understanding temporal and spatial patterns of distribution, abundance, and life-cycle biology, however, reflect the profound influences of varying environmental conditions. The need for further research on these topics increases as humankind faces the challenges of predicting the impacts of climate change and ocean acidification on the species. The increasing use of molecular methods of prey identification (based on amplifying and sequencing prey DNA) has the potential to provide a step change in our understanding of squid trophic relationships, and indeed such techniques already allow recognition of L. vulgaris in commercial food products (Herrero et al., 2012). This is relevant both to studies of L. vulgaris diet, the analysis of which currently relies on relatively scarce and difficult-to-identify hard remains, and studies on predators of squids, Cephalopod biology and fisheries in Europe: II. Species Accounts | 135 notably due to the near impossibility of distinguishing beaks of L. vulgaris and L. forbesii. It is evident from the great fisheries importance of this species and the poor taxonomic resolution of ICES and FAO fishery statistics that there is an urgent need for adequate recording of the species of squid landed in European fisheries. This is already achieved in some countries at local or regional levels, and Robin and Boucaud-Camou (1995) demonstrated that market sampling could be used to quantify month-to-month changes in the proportions of the two Loligo species in landings along the French coast of the English Channel. 136 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Loligo forbesii Veined squid Cephalopod biology and fisheries in Europe: II. Species Accounts 12 | 137 Loligo forbesii Steenstrup, 1856 Graham J. Pierce, Lee C. Hastie, Evgenia Lefkaditou, A. Louise Allcock, Jennifer M. Smith, Sansanee Wangvoralak, and Patrizia Jereb Common names Encornet veiné (France); Καλαμάρι [calamary] (Greece); calamaro venato, occhione (Italy); lula-riscada (Portugal), calamar veteado (Spain); veined squid, European northern squid (UK) (Figure 12.1). Synonyms Loligo fusus Risso, 1854, Loligo moulinsi Lafont, 1871. 12.1 Geographic distribution The veined squid, Loligo forbesii Steenstrup, 1856, is found in the Northeast Atlantic, from ca. 60N to ca. 20N, and throughout the Mediterranean (Jereb et al., 2010) (Figure 12.2). A neritic and mainly near-bottom species, it lives in coastal waters and continental shelf seas of the Northeast Atlantic, from the Faroe Islands (Howard, 1979; Gaard, 1987) and the northern North Sea (Howard et al., 1987) to the southwest coast of Norway (Grieg, 1933), where it has been recorded as far north as Trondjemsfjord (Nordgård, 1923). The species was considered Figure 12.1. Loligo forbesii. Dorsal view. From Roper et al. (1984). absent from the Baltic Sea by Roper et al. (1984) and Jereb et al. (2010), but old records exist of the species in the Kattegat and western Baltic Sea (Grimpe, 1925) and are supported by recent observations (Hornbörg, 2005), although the presence of the species is considered extremely variable in those areas. Loligo forbesii inhabits the central and southern North Sea (De Heij and Baayen, 2005; Oesterwind et al., 2010) and is common in British and Irish waters (Holme, 1974; Howard, 1979; Howard et al., 1987; Pierce et al., 1994b, 1998; Collins et al., 1995b). It also extends south through French and Spanish waters to the west coast of Africa, around and south of the Canary Islands, to ca. 23–24°N according to FAO (1979) or even to 18°N according to Roper and Sweeney (1981), and west to Madeira (Clarke and Lu, 1995) and the Azores (Martins, 1982). Although the southern limits of its distribution remain unknown (Guerra, 1992), the Azores Islands are considered its western limit in the Northeast Atlantic. Loligo forbesii has been recorded throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), although it is scarce in the northwestern Mediterranean, but more abundant in the Strait of Sicily (in the early 1990s) and in the northeastern Ionian Sea (Naef, 1921/1923; Mangold-Wirz, 1963a; Boletzky and Mangold, 1985; Ragonese and Jereb, 1986; Jereb and Ragonese, 1994; Lefkaditou et al., 2003a). Its occurrence in the Adriatic Sea is limited to central and southern areas (Casali et al., 1988; Bello, 1990; Krstulović Šifner et al. 2005), is found in the Aegean Sea and the Levant Basin (D’Onghia et al., 138 | ICES Cooperative Research Report No. 325 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b), but has not been recorded in the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Figure 12.2. Loligo forbesii. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 12.2 Taxonomy 12.2.1 Systematics Coleoidea– Decapodiformes –Myopsida – Loliginidae – Loligo. 12.2.2 Type locality North Sea, Denmark (exact position not known). 12.2.3 Type repository Kobenhavns Universitet, Zoologisk Museum, Universitetsparken 15, DK 2100 Copenhagen, Denmark. Syntype [fide Kristensen and Knudsen (1983)]. Loligo forbesii Steenstrup, 1856, Danske videnskabernes selskabs skrifter (5) 4:189. 12.3 Diagnosis 12.3.1 Paralarvae Hatchlings of this species are differentiated from their congener species Loligo vulgaris by their larger size; mean ML of L. forbesii hatchlings is 3.7 mm (range 3.5–4.9 mm) compared with 3.1 mm (2.8–3.3 mm) for L. vulgaris. Note, however, that hatchling size apparently varies regionally in L. vulgaris (González et al., 2010), and this may also be true for L. forbesii. The chromatophore patterns are highly variable, and the number of chromatophores decreases from the ventral to the dorsal side in hatchlings of both species. Fins are paddle-shaped, broad with short bases, and each fin is much wider than Cephalopod biology and fisheries in Europe: II. Species Accounts | 139 long. The tentacular clubs are broad and much wider than the tentacular stalks (Segawa et al., 1988; Hanlon et al., 1989; Sweeney et al., 1992; Yau, 1994). 12.3.2 Juveniles and adults The body form of juveniles is bullet-shaped, with well-developed, paddle-shaped, terminal fins. The ventral arms and tentacles are also well developed, and the tentacular club suckers are like those of the adult, i.e. median suckers slightly larger (1.5-fold) than marginal suckers (Yau, 1994). The mantle of adults is long, moderately slender, muscular, and cylindrical; the fins are rhomboid, with slightly concave posterior borders, and their length is ca. 75% the length of the mantle. A cornea covers the eye. The arms have two series of suckers. The species lacks the markedly enlarged medial suckers typical of the tentacular club of L. vulgaris. Instead, the suckers on the manus of the tentacular club of L. forbesii are subequal in size (Figure 12.3). The sucker rings on the tentacular club have 13–18 Figure 12.3. Details of the tentacular clubs sharp conical teeth. The largest sucker rings of L. forbesii (above) and L. vulgaris (beon the arms have 7–8 teeth. In mature males, low), showing the enlarged central series the left ventral arm (IV) is hectocotylized in of suckers in L. vulgaris. Photo: Andy Lucas its distal third by modification of suckers into long papillae that gradually decrease in size distally. The locking cartilage is simple (Naef, 1921/1923; Roper et al., 1984; Guerra, 1992; Jereb et al., 2010). Loligo forbesii has “prominent longitudinal flame-like stripes of purplish dark chromatophores on the anterior and ventrolateral surfaces of the mantle” (Jereb et al., 2010), although Holme (1974) describes them as orange-red in colour. This feature is also sometimes seen in large mature males of L. vulgaris, although the stripes are usually much smaller and less numerous. In general, the mantle colour is more orange in L. forbesii and more violet or purple in L. vulgaris (Figure 12.4). 12.4 Life history The life cycle of L. forbesii is annual, and maximum lifespan is ca. 16 months. It usually spawns in winter, but summer breeders have also been described in some areas. 12.4.1 Egg and juvenile development The size of the egg string or egg size itself is generally used to distinguish L. forbesii eggs from those of L. vulgaris (Naef, 1921/1923; Sacarrão, 1956–1957; Boletzky, 1987b). The egg strings of L. forbesii are larger and contain fewer eggs of greater volume than those of L. vulgaris (Martins, 1997). Grimpe (1925) stated that L. forbesii egg strings contain an average of 54 eggs, ca. half the number of eggs in L. vulgaris egg strings. However, Holme (1974) found egg strings to contain 50–130 eggs per string. Eggs of L. forbesii are large and supplied with a large quantity of yolk relative to many marine fish eggs (Boletzky, 1987b; Hanlon et al., 1989). They are packed and wrapped in gelatinous substances produced by the oviducal and nidamental glands, forming finger-like 140 | ICES Cooperative Research Report No. 325 egg strings. The number of egg strings in a cluster is variable, and a cluster may contain egg strings spawned and deposited by one or several females. A single egg string may be fertilized by more than one male and hence be multipaternal (Shaw and Boyle, 1997). Clusters of these egg strings are normally attached to substrata that include algae, shells, rock crevices, nets, ropes, creels, and other fishing gear (e.g. Holme, 1974; LumKong et al., 1992). Figure 12.4. External appearance of large, mature males of Loligo forbesii (above) and L. vulgaris (below), showing the more prominent “flame-like” stripes on the mantle of the former. These two specimens were caught in Scottish waters in early 1990. Differences in colouration of the mantle and stripes are also evident. Photo: Andy Lucas. Records of egg masses of L. forbesii originate primarily from inshore areas. Collins et al. (1995c) recovered egg masses from static fishing gear over rocky ground at 10–50 m off the south coast of Ireland. There are numerous incidental and anecdotal records of egg masses attached to fixed fishing gear in UK waters at various times of year, and Holme (1974) reported egg masses attached to fishing floats, rope moorings, and crab pots in inshore areas off the coast of Plymouth. Lum-Kong et al. (1992), Martins (1997), and Craig (2001) found egg masses attached to inshore creel lines in Scottish waters over muddy and rocky substrata in depths of 30–110 m in both winter and summer. Fishers interviewed about the distribution of squid in the Moray Firth (North Sea coast, UK) reported egg masses from all around their coast in water as shallow as 2 m along moorings and piers, but also from the middle of the Moray Firth attached to creel lines (Smith, 2011). Regardless of distance from the coast, egg masses in the Moray Firth tend to be found over rocky bottoms. Lordan and Casey (1999) argue that the species is more likely to spawn over rocky bottoms where opportunities to attach eggs to the substratum are more numerous. In Portugal, based on the distribution of spawning females, egg strings of L. forbesii are believed to be deposited farther offshore than those of L. vulgaris (Cunha et al., 1995). Recently, an L. forbesii egg mass was recovered on the west coast at 240 m (A. Moreno, pers. comm.). From egg masses recovered on octopus traps, spawning activity in the Azores is known to take place at depths of 25–144 m (Porteiro and Martins, 1992; Pham et al., 2009). The deepest record of an egg mass of this species in the Azores, and the only record from the area to date not obtained from fish traps, was a group of 2–30 egg strings seen in a rocky crevice at 373 m depth using an ROV (Carreira et al., 2011). Cephalopod biology and fisheries in Europe: II. Species Accounts | 141 Lum-Kong et al. (1992) suggested that most spawning could take place outside coastal waters because commercial samples containing fully mature squid originate largely from fishing areas some distance from the coast. Although several records point to spawning in deeper waters of both the Atlantic and Mediterranean (e.g. Lordan and Casey, 1999; Salman and Laptikhovsky, 2002; Carreira et al., 2011), the general lack of data on eggs from such areas could be due to egg masses trawled offshore going unreported and/or the preference of squid spawning over rocky substratum, making spawning areas largely inaccessible to trawling (Holme, 1974; Lordan and Casey, 1999). The deepest record to date (730 m) is one from the Aegean Sea (eastern Mediterranean; Salman and Laptikhovsky, 2002), at a bottom water temperature of 13°C. Observations in captivity show that the timing of development and hatchling emergence of L. forbesii depends on both egg size and temperature (Paulij et al., 1990b; Gowland, 2002). Size at hatching varies inversely with temperature and is significantly less at 16C than at 8C. Duration of the embryonic phase increases as temperature decreases: 140 d at 8C, 60 d at 12C, and 36 d at 16C (Martins, 1997; Gowland et al., 2002). Growth patterns also change with varying temperature. Hatchlings reared at 12C have long, narrow mantles consistent with normal development, whereas hatchlings reared at both higher and lower temperatures have shorter and wider mantles. Craig (2001) found that all hatchlings emerged during darkness. Hatchlings from each string emerge over a period of ≥2 days. At hatching, L. forbesii paralarvae exhibit positive phototaxis, and swim actively. From 2 d on, swimming near the surface is rare (Martins, 1997). The statolith shape of L. forbesii hatchlings is different from that of juveniles (>50 mm ML) and adults. Martins (1997) postulated that if changes in swimming behaviour (ontogenetic descent, dexterity, and velocity) were related to changes in statolith shape, then the stage at which the form of the statolith changes could be indicative of the end of the planktonic life phase. However, Collins et al. (2002) suggested that the general absence of this species from plankton samples could indicate that the paralarva is not planktonic. Using an epibenthic sled, Robin and co-workers caught hundreds of squid paralarvae in the English Channel during surveys in June 2011 and March 2013, mostly Alloteuthis and a few L. vulgaris, but no L. forbesii paralarvae (J.-P. Robin, pers. comm.). Statolith length is highly correlated with dorsal mantle length, larger hatchlings having larger statoliths. Gowland (2002) found that deformities in hatchlings increased with increasing temperature, whereas Martins (1997) found more deformed hatchlings in L. forbesii acclimated to temperatures <13C. This suggests a relatively narrow temperature optimum for normal hatchling development. Deformities in development may also be caused by hypoxia or abnormal ion concentrations (Hanlon et al., 1989). Detailed descriptions of embryonic stages of L. forbesii can be found in Segawa et al. (1988). 12.4.2 Growth and lifespan Loligo forbesii is one of the largest members of the family Loliginidae. Male L. forbesii can grow considerably larger and heavier than females and have faster growth rates. Typically, adult body size reaches 100–650 mm ML in males (weight range 155–3700 g) and 175–350 mm ML in females (weight range 200–1150 g) throughout the species’ range. However, there is wide variation within both sexes and, in particular, some males mature at ca. 120 mm long and probably never grow much larger (Pierce et al., 1994c; Porteiro and Martins, 1994; Boyle et al., 1995). Females as large as 420 mm ML and 1.5 kg and males of 735 mm and 4.3 kg have been recorded in Scottish waters (G. J. Pierce, pers. comm.). In the Azores population, males 142 | ICES Cooperative Research Report No. 325 reach 937 mm ML and 8.3 kg, compared with 462 mm ML and 2.2 kg for females (Martins, 1982). Genetic differences between the Azores and mainland coastal samples indicate that the former may represent a separate subspecies (Brierley et al., 1995; Shaw et al., 1999). However, the large size of squid observed in Azorean waters may also be at least partly due to sampling bias, because the squid sampled in the above-mentioned studies were caught by jigging. Very large individuals (males >500 mm ML) appear occasionally in commercial trawl catches landed in other areas, e.g. the records for Scotland, and a large male of 560 mm ML found at the fish market in Sicily (Jereb and Ragonese, 1986), but it is not certain that they are as rare as they appear to be, because they may simply not often be caught by trawling. Several techniques have been used to determine the growth characteristics of L. forbesii, including observations in captivity (Forsythe and Hanlon, 1989), length frequency analysis (Pierce et al., 1994c), and estimates based on growth increments in the statoliths (Collins et al., 1995c) and the gladius (Hughes, 1998). The gladius extends the entire length of the mantle, and a growth increment of 1 mm in the gladius therefore represents ca. a 1-mm increase in mantle length. Modal progression analysis of length frequency data, whereby the growth of putative cohorts is followed through most of the post-recruit life cycle, along with plotting of maturity ogives, has revealed the presence of two or more size modes at maturity, apparently corresponding to different growth strategies, in both sexes (Holme, 1974; Boyle and Ngoile, 1993a; Pierce et al., 1994c; Boyle et al., 1995; Collins et al., 1995c, 1999). Males consistently exhibit at least two alternative growth strategies, with some maturing very small; these probably correspond to different reproductive strategies: mateguarding by large males and sneaking by small males (Hanlon and Messenger, 1998). However, some studies have suggested as many as 3–4 cohorts (or “microcohorts”), with different growth trajectories in males and 2–3 in females (e.g. Collins et al., 1999). It should be noted, however, that reliable resolution of multiple modes in length frequency data requires large samples and regular sampling. Boyle et al. (1995) suggested that the different size modes in mature males of this species could reflect differences in age or growth rate and could be of environmental or genetic origin. Wangvoralak (2011) showed that if males sampled in Scotland during 2007–2008 were divided into two groups based on hatching dates, evidence of two sizes at maturity was then seen only in animals hatched in cold months and not in those hatched during warm months. The same author showed that maturity ogives calculated in terms of age rather than length were simpler in form, with no evidence of two modes, i.e. that all individuals tended to mature at similar ages. Temperature is known to affect the development time of embryos (Boletzky, 1987b). The development time of L. forbesii is 75 d at 12.5°C (Hanlon et al., 1989). Based on the report of a viable egg mass remaining at a particular site for 6 months at temperatures of 8–10°C, Boyle et al. (1995) suggested that, in Scottish waters, the development of L. forbesii eggs may be held in stasis over the coldest period of winter, generating two cohorts from a single breeding population with an extended spawning period. Statoliths of L. forbesii were first used for age determinations by Martins (1982); subsequent studies include those by Gaard (1987), Guerra and Rocha (1994), Collins et al. (1995c), Hughes (1998), Rocha and Guerra (1999), and Wangvoralak (2011). Increments in squid statoliths are proposed to be formed daily (Kristensen, 1980; Lipiński, 1986, 1993; Rodhouse and Hatfield, 1990). In L. forbesii, daily deposition of statolith increments has been validated in aquarium-based studies (Hanlon et al., 1989), and has been supported by increment counts in statoliths of squid from successive monthly fishery Cephalopod biology and fisheries in Europe: II. Species Accounts | 143 samples (Collins et al., 1995c). Based on the results from counting growth increments on statoliths (Gaard, 1987; Guerra and Rocha, 1994; Boyle et al., 1995; Collins et al., 1995c; Rocha and Guerra, 1999; Wangvoralak, 2011) and aquarium studies (Hanlon et al., 1989), there is general consensus that L. forbesii can live 15–16 months, with most sampled animals being no more than a year old. The largest male recorded in Scotland to date (ML = 735 mm) was estimated to be 420 d old (i.e. ca. 14 months; G. J. Pierce, pers. comm.). The growth pattern in loliginid squid appears to comprise two distinct phases: an early rapid, “exponential” phase, followed by a secondary, slower, “logarithmic” phase (Forsythe and van Heukelem, 1987; Forsythe and Hanlon, 1989). During the exponential phase, juvenile L. forbesii can achieve daily growth rates of 8% of body mass (Forsythe and Hanlon, 1989; Grist and Des Clers, 1998). However, that phase generally lasts no more than 2–4 months (Jackson, 1994). Over the course of the life cycle, growth rate gradually declines, from 5.4% BW d–1 in the smallest individuals to 1.4 in the largest (Forsythe and van Heukelem, 1987). Forsythe and Hanlon (1989) give the final growth rate as 1–2% BW d–1. Based on statolith data collected from post-recruit animals, Collins et al. (1995c) reported growth rates of 0.98% ML d–1 and 2.48% BW d–1 in males, and 0.85% ML d–1 and 2.26% BW d–1 in females. This corresponded to growth of ca. 1 mm d–1 for females and 1–5 mm d–1 for males. Growth rates estimated from modal progression analysis using monthly length frequency data were slightly lower (e.g. female growth rate was 30 mm month–1 from statoliths and 15–30 mm month–1 from length frequency data). Individual growth rates in squid are highly variable, as revealed by both rearing studies and analysis of market sample data on length, weight, age, and gladius increments. Factors affecting growth rate include food availability and water temperature, as well as sex, maturity, season, and hatching time (Forsythe and van Heukelem, 1987; Rodhouse and Hatfield, 1990; Bettencourt et al., 1996; Hughes, 1998; Smith et al., 2005, 2011; Wangvoralak, 2011). Cephalopods are poikilotherms and, as such, temperature is thought to be one of the main external factors determining growth rate prior to sexual maturity, although the logarithmic phase is apparently less temperature-dependent than the earlier exponential phase (Forsythe, 1993; Grist and Des Clers, 1998). In captivity, when food is not limited, temperature is positively related to growth rate up to optimal values (Forsythe and van Heukelem, 1987). However, squid that experience colder temperatures prior to hatching may ultimately attain adulthood at larger size (and/or older ages) (Wangvoralak, 2011). Comparisons of length–weight relationships from different studies (see Table 12.1) are generally difficult, in this species as in many others, because of the use of different length–weight models, the fact that confidence limits are rarely indicated, and, often, an absence of information on the model fitting-procedures. Nevertheless, it is clear that there are sex-related differences in the length–weight relationship (Holme, 1974; Martins, 1982; Gaard, 1987; Ngoile, 1987; Boyle and Ngoile, 1993b; Pierce et al., 1994c; Guerra and Rocha, 1994; Moreno et al., 1994). Although there is some overlap in values for the exponent b, it is consistently higher in females (b = 2.18–2.66) than in males (b = 2.00–2.58), indicating that female L. forbesii are relatively heavier at a given length. This feature has also been noted in L. vulgaris (Coelho et al., 1994; Guerra and Rocha, 1994; Moreno et al., 2002). Table 12.1. Loligo forbesii. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g), ML is dorsal mantle length (cm), and a and b are the coefficients. 144 | ICES Cooperative Research Report No. 325 Region a b Sex Reference Faroe Islands 0.074– 2.61– F Gaard (1987) 0.088 2.66 0.133– 2.30– 0.180 2.45 0.113 2.61 F 0.175 2.43 M Scotland 0.201 2.33 All Young et al. (2004) Scotland west coast 0.151 2.51 F Ngoile (1987) 0.214 2.37 M 0.138 2.49 F Rockall (ICES Division VIb) Scotland M Ngoile (1987) Boyle and Ngoile (1993b) Scotland Northern North Sea Middle North Sea English Channel Northwestern Spain 0.192 2.36 M 0.151 2.43 F 0.206 2.29 M 0.161 2.53 F 0.268 2.33 M 0.164 2.45 F 0.232 2.55 M 0.449 2.43 F 0.527 2.29 M 0.111 2.57 F Pierce et al. (1994c) Ngoile (1987) Ngoile (1987) Holme (1974) Guerra and Rocha (1994) Portugal Portugal Azores Northeastern Mediterranean 0.138 2.44 M 0.102 2.60 F 0.103 2.58 M 0.104 2.59 F 0.111 2.54 M 0.425 2.18 F 0.548 2.08 M 0.141 2.46 All Sea 12.4.3 Moreno et al. (1994) Cunha (2000) Martins (1982) E. Lefkaditou, pers. comm. Maturation and reproduction There seems to be an annual cycle in the sex ratio, females being more abundant than males during the spawning season, e.g. November–February in Scotland. There is also evidence of males outnumbering females during the recruitment period in Scotland and Spain (Holme, 1974; Guerra and Rocha, 1994; Pierce et al., 1994c; Collins et al., 1999). Holme (1974) speculated that large males are better able to avoid trawls, but Collins et al. (1999) indicate that abundance of males declines earlier than that of females in the breeding season. The maturation process in L. forbesii is affected by both intrinsic factors (e.g. age, body size, and sex) and external factors (e.g. hatching season, temperature, daylight, food supply). In Scottish waters, gonad weight in both sexes is related to calendar month, consistent with seasonal triggering of maturation, and to digestive gland weight, indicating an effect of nutritional status, as might be expected if energy for gonad growth is derived primarily from food (Smith et al., 2005). Once animals have reached maturity, Cephalopod biology and fisheries in Europe: II. Species Accounts | 145 there is evidence of a decline in gonad growth in males, whereas females apparently continue to invest energy to grow gonads (Wangvoralak, 2011), presumably because eggs continue to grow and mature within the ovary. As noted above, male L. forbesii exhibit at least two different growth and reproduction strategies, individuals maturing over two different size ranges (Guerra and Rocha, 1994; Moreno et al., 1994; Boyle et al., 1995; Collins et al., 1995d), although apparently at similar ages (Wangvoralak, 2011), and a similar phenomenon is sometimes encountered in females. As a consequence, standard population reproductive parameters such as size-at-50%-maturity (MLm50%) can be misleading, at least in males. Published results on the range of size at maturity, nevertheless, make clear the variability of the growth and maturation process (Table 12.2). Loligo forbesii has an annual life cycle and is generally described as semelparous (LumKong et al., 1992; Pierce et al., 1994c; Collins et al., 1995d), with an extended spawning season or ”intermittent, terminal spawning”, i.e. the females lay eggs in batches and die shortly after completion of spawning (Rocha et al., 2001). The timing of peak spawning activity varies across the range, and additional peaks are observed in some areas (Roper et al., 1984; Lum-Kong et al., 1992; Boyle and Ngoile, 1993a; Guerra and Rocha, 1994; Moreno et al., 1994; Pierce et al., 1994c; Boyle et al., 1995; Collins et al., 1995d), possibly because of the presence of both winter and summer breeders (Holme, 1974). In Scottish waters, L. forbesii spawns mainly in December–February, although at least some mature specimens can be found throughout the year (Pierce et al., 1994c). Demersal trawl survey results from 2004 (Stowasser et al., 2005) indicated that the greatest abundance of L. forbesii in autumn was along the shelf edge west of Scotland and Ireland. As the spawning season progressed (January–March), locations of high squid abundance shifted from offshore to inshore, with abundance greatest in the Minch (northwestern Scotland) and Moray Firth (northeast Scotland) and south along the east (North Sea) coast of the UK. Table 12.2. Reported ranges of size-at-maturity for male and female L. forbesii (from size at first detection of maturity to 100% of sample mature). Where multiple microcohorts were detected, separate estimates are given for each. Area Male ML (mm) Female ML (mm) Reference Faroe Islands 200–250 180–200 Gaard (1987) 220 Howard (1979) 120–450 160–310 Boyle et al. (1995) Scotland (west 180–220, 250– 180–220, 280–320 Collins et al. (1999) coast) 320, >400 Scotland (North Sea) 180–350 192–250 Wangvoralak (2011) Ireland 120–400 150–300 Collins et al. (1995a) England (southwest) 130–420 160–320 Holme (1974) Galicia (northwestern 160–380 160–380 Guerra and Rocha Scotland + Faroe Islands Scotland (west coast) Spain) (1994) Portugal 145–450 175–315 Moreno et al. (1994) Azores Islands <310–490 <250–326 Martins (1982) Azores Islands <240–611 <200–390 Porteiro and Martins (1994) 146 | ICES Cooperative Research Report No. 325 In summer, mature specimens were found only in the English Channel. In an analysis of historical data, Pierce et al. (2005) found high autumn/winter temperatures (high winter NAO values) to be associated with high squid abundance and precocious maturation, which tended to favour high abundance in the following year, along with increased body weight at length and a decrease in the proportion of animals breeding in December. High abundance in summer, conversely, was correlated with lower body weight at length the following year. Pham et al. (2009) were the first to describe spawning behaviour of this species in the wild and noted that the “chromatic, locomotor and postural components were very similar to those of other coastal loliginids observed on spawning grounds”. They describe a range of behaviours including “‘pair formation’, ‘mate guarding’, ‘egg holding’, ‘egg touching’, ‘white arms’, ‘red accessory nidamental glands’, ‘accentuated testis’, and ‘jockeying and parrying’”. Although they are relatively short-lived species, fecundity in loliginid squids is surprisingly low. Female L. forbesii apparently produce only a few thousand eggs in their lifetime (Boyle et al., 1995). Mature females exhibit asynchronous oocyte maturation, with oocytes found in various stages of development at any one time (Ngoile, 1987; Collins et al., 1995a). The number of oocytes present (or potential fecundity) in L. forbesii females has been estimated to range from 1000 to 23 000 eggs (Guerra and Rocha, 1994; Boyle et al., 1995). A weak positive relationship between ML and potential fecundity is reported, although small mature females may have relatively more oocytes than larger females as a proportion of body weight (Boletzky, 1987b; Hanlon et al., 1989; Guerra and Rocha, 1994; Boyle et al., 1995; Collins et al., 1995a). 12.5 Biological distribution 12.5.1 Habitat Jereb et al. (2010) indicate that the species can be found down to >700 m, based on captures from bottom-trawl surveys in the Sicilian Channel and records of egg masses, both in the Mediterranean and Atlantic. The main population in UK waters is distributed over the continental shelf and shelf edge, mostly in water 50–250 m deep and within ca. 200 km of the coast (Pierce et al., 1994b). Oesterwind et al. (2010) recorded L. forbesii at depths of 20–171 m in the North Sea during bottom-trawl surveys. At Rockall Bank, 200 miles west of Scotland, survey catches were mostly in shallow water <150 m (Pierce et al., 1998). Moreno et al. (1994) reported L. forbesii at depths of 100–200 m in Portuguese waters. Mangold-Wirz (1963a) described the vertical distribution of L. forbesii as between 15 to 150 m in the North Sea and eastern Atlantic, and 150–400 m in the Mediterranean. Several published records show that the species can extend into deeper water. Lordan and Casey (1999) found egg masses at ca. 500 m depth in the Celtic Sea, Ragonese and Jereb (1986) reported L. forbesii to be commonly captured at 560 m depth in the Sicilian Channel, Salman and Laptikhovsky (2002) recorded egg masses at a depth of 730 m in the Aegean Sea, Lefkaditou et al. (2003a) refer to its capture at 715 m in the Ionian Sea, and Orsi Relini et al. (2009) report an egg mass from 600 m in the Ligurian Sea. In the Azores, the species is recorded over water depths >1000 m, although such depths are close to the coast, and there is no published evidence that the species descends to the seabed at such depths; it is normally fished near the surface by jigging (Martins, 1982). Where its distribution overlaps with that of L. vulgaris, L. forbesii tends to be found in deeper water. According to Ragonese and Jereb (1986), in the Sicilian Channel (central Cephalopod biology and fisheries in Europe: II. Species Accounts | 147 Mediterranean), the switch from dominance by one species to the other is at ca. 70–80 m; L. vulgaris was seldom found deeper and L. forbesii was never captured shallower. A similar situation is described by Ria et al. (2005) in the southern Ligurian Sea (Mediterranean), where L. forbesii is found at depths of 80–600 m, whereas L. vulgaris is in shallow coastal waters (<60 m depth). Studies on temporal trends in abundance of L. forbesii in UK waters show that both the timing of migration into the English Channel and winter abundance in the North Sea are related to sea surface temperature (SST) (Pierce et al., 1998; Waluda and Pierce, 1998; Sims et al., 2001; Pierce and Boyle, 2003). Squid abundance in the English Channel peaks when bottom temperature is 13C, independent of time of year (Sims et al., 2001). Zuur and Pierce (2004) found that squid abundance was related to both strength of the North Atlantic Oscillation (NAO) and SST, proposing that both the inflow of Atlantic water (with associated nutrients, prey organisms, and squid) and favourable growth conditions (i.e. temperature) are important in determining abundance, as measured by catch per unit effort. The distribution of L. forbesii in the North Sea in winter seems to be strongly correlated with seabed temperatures (SBT) and, to a lesser extent, salinity (i.e. more squid in more saline waters), with L. forbesii generally not being found at temperatures <7C (Pierce et al., 1998). Bellido et al. (2001) found that commercial fishery catch rates of L. forbesii in UK waters were best when SST was ca. 11C. Oesterwind et al. (2010) found L. forbesii at temperatures (SBT) of 6.3–9.4C in winter and 8.1 and 18.2C in summer in the North Sea. In Portuguese waters, catches of loliginid squid were best when SST was in the range 13–16C (Moreno and Sousa-Reis, 1995). Georgakarakos et al. (2002) found a positive correlation between loliginid landings and SST in nutrient-rich areas. 12.5.2 Migrations Migratory patterns have been described for the species, but are poorly understood. One issue is the low spatial and temporal resolution of data available from both trawl surveys and commercial fisheries (trawl surveys tend to include only a single haul per ICES rectangle, and commercial catch data are normally aggregated to this spatial scale). In addition, movements have been inferred from shifts in distribution rather than directly observed and, finally, there is evidence that distribution and movements vary between years (see Waluda and Pierce, 1998; Viana et al., 2009). Several authors have reported evidence of inshore–offshore movement associated with the breeding cycle in Scottish waters (Pierce et al. 1998; Stowasser et al., 2005; Viana et al., 2009), and there is also evidence of movements parallel to the coast in several regions (Holme, 1974; Waluda and Pierce, 1998; Sims et al., 2001; Oesterwind et al., 2010). Most evidence seems to suggest that post-hatching L. forbesii migrate away from the coast, moving offshore as they grow, but subsequently returning to shallow water to breed. There are few records of capture of post-spawning squid, and it is most likely that they die soon after spawning, although post-breeding offshore migration of adults has also been proposed. Holme (1974) reported that L. forbesii hatched in the western English Channel and migrated east, appearing in trawls off Plymouth around May. After a few months of rapid growth in the English Channel and the southern North Sea, the squid moved back to the Western Approaches to spawn, and died during the following December–January (although he also noted the presence of summer spawners). Sims et al. (2001) showed that the annual timing of the arrival of L. forbesii in trawls off Plymouth varied according to sea temperature. 148 | ICES Cooperative Research Report No. 325 Waluda and Pierce (1998) interpreted month-to-month trends in catch locations from UK fishery data as implying west–east migrations over the course of the breeding cycle, with squid moving from deeper water in the west to spawn in coastal water in the east, subsequently moving offshore again. However, subsequent analysis of commercial fishery catch data for Scotland, from a longer series of years, by Viana et al. (2009) indicated that inshore–offshore movements with no important east–west component were more common. Distribution maps based on trawl survey data collected by Scottish vessels during the years 1980–1994 confirm the existence of centres of abundance north of Shetland and at ca. 56N in both February and April, whereas the only centre of abundance in August and October was around the Moray Firth (Pierce et al., 1998). These findings are consistent with observations by fishers that high concentrations of juveniles are found close inshore in the Moray Firth (Scotland) in summer, where they are targeted by a small directed fishery (Young et al., 2006a, b). Trawl survey data from UK waters for 2004–2005 showed that squid were predominantly found in deeper water along the shelf edge (100–200 m) at the beginning and end of the winter spawning season (November and March), and that most squid were caught in water shallower than 50 m during the peak of winter spawning (Stowasser et al., 2005). Trawl survey data from 2007 to 2009 indicate that L. forbesii concentrate mainly in the northern part of the North Sea in winter, especially around Shetland, and that the centre of abundance shifts south to ca. 56N in summer (Oesterwind et al., 2010). 12.6 Trophic ecology 12.6.1 Prey Loligo forbesii is a highly mobile, opportunistic predator that will attack and consume any potential prey that it can overcome (including members of its own species). Dietary studies have covered various parts of its range, including the UK (Ngoile, 1987; Pierce et al., 1994a; Collins and Pierce, 1996; Pierce and Santos, 1996; Stowasser, 1997, 2004; Wangvoralak et al., 2011), Ireland (Collins et al., 1994; Collins and Pierce, 1996), Spanish Atlantic waters (Pierce et al., 1994a; Rocha et al., 1994), and Portugal (Martins, 1982; Porteiro et al., 1990; Pierce et al., 1994c). A large number of different prey species, including various fish, crustaceans, and cephalopods, as well as polychaetes and other molluscs, have been identified in L. forbesii stomachs (Table 12.3). In most locations, fish are the main prey, with crustacean, cephalopod, and polychaete species also present in the diet to varying degrees. The most prominent fish species in the diet belong to the families Gadidae, Clupeidae, Ammodytidae, and Gobiidae (Collins et al., 1994; Rocha et al., 1994; Collins and Pierce, 1996; Pierce and Santos, 1996; Wangvoralak et al., 2011). There are ontogenetic shifts in diet, from a crustacean-dominated one in juvenile squid to a predominance of fish in the diet of adult squid (Pierce et al., 1994a). Rearing studies showed L. forbesii paralarvae to feed mainly on copepods, juvenile mysids, and palaemonid larvae (Forsythe and Hanlon, 1989; Hanlon et al., 1989). In Spanish waters, cephalopods also make up a greater component of the diet of L. forbesii as the squid grow (Rocha et al., 1994). Cannibalism in L. forbesii appears to be limited to large squid (>150 mm ML) feeding on much smaller ones (20–50 mm ML) (Collins et al., 1994). The same broad prey taxa are important in the diet of L. forbesii throughout its geographic range (Pierce et al., 1994a). However, regional differences in the diet have also Cephalopod biology and fisheries in Europe: II. Species Accounts | 149 been identified. For example, in Scottish waters, whiting (Merlangius merlangius), Trisopterus spp., and sandeels (Ammodytidae) are the principal fish prey (Pierce et al., 1994a), whereas in Irish waters, the dominant prey species are sprat (Sprattus sprattus) and Trisopterus spp. (Collins et al., 1994). Prey composition may vary seasonally, probably because of changes in prey availability (Collins et al., 1994; Pierce et al., 1994a; Rocha et al., 1994). No significant differences have been found between the diets of male and female L. forbesii (Pierce et al., 1994a; Rocha et al., 1994) or animals of different maturity stages (Rocha et al., 1994). However, Howard et al. (1987) observed seasonal differences in stomach emptiness, with a higher frequency of empty stomachs in winter, and Gaard (1987) noted that L. forbesii probably feeds mainly by day, because full stomachs and less-digested contents were more frequent in samples taken in the evening. Rocha et al. (1994) observed more empty stomachs in immature females than in mature females and in mature females than in mature males. Investigations into the trophic ecology of L. forbesii through fatty-acid and stable-isotope analysis have shown that L. forbesii is mainly associated with the benthic foodweb and also confirmed that both diet composition and dietary variability change with increasing body size. Application of these methods has also made it possible to infer ontogenetic movements from offshore to more coastal waters and to determine the diet of individuals that have no food in their stomachs (Stowasser, 2004). Chouvelon et al. (2011) reported a positive correlation between δ15N values and ML in this species, implying an ontogenetic trend of increasing prey size (and trophic level). Table 12.3. List of identified prey types and species from Loligo forbesii stomach contents (compiled from Martins, 19821; Collins et al., 19942; Guerra and Rocha, 19943; Pierce et al., 1994a4; Stowasser, 19975, 20046; Hastie et al., 2009a7; Wangvoralak et al., 20118). Taxon Species Osteichthyes Agonidae Agonus cataphractus (hooknose)2 Ammodytidae Ammodytes marinus (lesser sandeel)8, Ammodytes spp.2,4,5,8, Gymnammodytes semisquamatus (smooth sandeel)3, Hyperoplus lanceolatus (greater sandeel)8, indet.2,3,4 Argentinidae Argentina silus (greater argentine)8, Argentina sphyraena (argentine)2,3,8, Argentina spp.4, indet.2 Atherinidae Atherina spp.3 Belonidae Belone belone (garfish)1 Bothidae Arnoglossus laterna (Mediterranean scaldfish)8 Callionymidae Callionymus lyra (dragonet)2,3,8, C. maculatus2, Callionymus spp.3,4,8, indet.2,5 Caproidae Capros aper (boarfish)1,4 Carangidae Trachurus picturatus (blue jack mackerel)1,8, T. trachurus (Atlantic horse mackerel)2,3,4,5, Trachurus spp.4 Centriscidae Macroramphosus scolopax (longspine snipefish)4 Cepolidae Cepola macrophthalma (red bandfish)2,3 Clupeidae Clupea harengus (Atlantic herring)2,4,5,6, Sardina pilchardus (European sardine or pilchard)3, Sprattus sprattus (European sprat)2,5, indet.2,4,5,8 Cyclopteridae Cyclopterus lumpus (lumpfish)4 150 | ICES Cooperative Research Report No. 325 Gadidae Gadiculus argenteus (silvery pout)2,4,6, Gadus morhua (Atlantic cod)4,5,8, Melanogrammus aeglefinus (haddock)4,5,8, Merlangius merlangus (whiting)2,4,5,8, Micromesistius poutassou (blue whiting)3,4,5,8, Phycis phycis (forkbeard)1, Pollachius virens (saithe)4, Trisopterus esmarkii (Norway pout)2,5,8, T. minutus (poor cod)2,8, Trisopterus spp.2,3,4,5,6,8, indet.2,3,4,5,6,8 Gobiidae Aphia minuta (transparent goby)2,3,6,8, Crystallogobius spp.3, Lesueurigobius friesii (Fries’ goby)2, Gobiusculus flavescens (two-spotted goby)8, Gobius niger (black goby)2, Pomatoschistus minutus (sand goby)2,3, Pomatoschistus spp.3,8, indet.2,3,4,5,6,8 Lotidae Enchelyopus cimbrius (four-bearded rockling)2,8, indet.4 Merlucciidae Merluccius merluccius (European hake)3 Pholidae Pholis gunnellus (rock gunnel)8 Pleuronectidae Hippoglossoides platessoides (Long rough dab)8, Pleuronectes platessa (European plaice)2, indet.2 Scombridae Scomber scombrus (Atlantic mackerel)4, Scomber spp.4 Sebastidae Helicolenus dactylopterus (blackbelly rosefish)4, Sebastes norvegicus (as S. marinus) (Norway redfish)4 Serranidae Anthias anthias (swallowtail seaperch)1 Sparidae Boops boops (bogue)1 Sternoptychidae Maurolicus muelleri (pearlside)2,4 Trichiuridae Lepidopus caudatus (silver scabbardfish), indet.1,4 Triglidae Eutrigla gurnardus (grey gurnard)2, indet.2 Chondrichthyes Etmopteridae Crustacea Decapoda Dendrobranchi- Etmopterus spp.1 indet.4 indet.5,6,8 indet.1 ata-Penaeiodea Pleocyemata- Paguridea indet.2 Anomura Pleocyemata- Maja spp.1, indet.1,3 Brachyura Pleocyemata-Car- Crangonidae indet.2, Dichelopandalus bonnieri2, Hippolytidae idea indet.3, Oplophoridae indet.2, Palaemonidae indet.2,5, Pandalidae indet.5,6, Pasiphaea sivado2, Processidae indet.3, indet.3 Macrura reptan- Nephrops norvegicus (Norway lobster)2 tia-Astacidea Euphausiacea Meganyctiphanes norvegica, indet.1,2,3,6 Mysida indet.3 Amphipoda indet.1,5 Cumacea Dyastilidae spp.5 Isopoda Cymothoida Gnathiidae spp.5, Gnathia spp. (larvae)2 Copepoda Calanoidea Cephalopoda Calanoidae spp.5,6, Temora turbinata8, indet.3 Cephalopod biology and fisheries in Europe: II. Species Accounts Myopsida | 151 Alloteuthis subulata3,4, Alloteuthis spp.3, Loligo forbesii1,4, L. vulgaris3, Loliginidae indet.2 Sepioidea Sepiolidae indet.2, Sepiola spp.5, Sepietta spp5., indet.4 Octopoda Eledone cirrhosa5, Octopus vulgaris3, Octopodidae indet.2,5, in- Teuthida det.1,2,4 Ommastrephidae indet.5 Gastropoda Calliostoma zizyphinum2, indet.2 Bivalvia Chlamys spp.2, indet.3 Nematoda indet.6 Polychaeta indet.4,5 Phyllodocida Nereis pelagica2, Nereis spp.8, Nereidae indet.1 Terebellida Sternaspidae indet.1 Chaetognatha Sagittoidea Sagitta spp.1 Foraminifera Miniacina spp.1 Bryozoa indet.1 Algae indet.2 12.6.2 Predators Loligo forbesii forms a component of the diet of a number of marine predators including some large demersal fish and marine mammals (Table 12.4). The great skua (Catharacta skua) is the only bird species from Northeast Atlantic waters for which beaks of Loligo sp. have been reported in its stomach contents (Furness, 1994), but because sampling was carried out in Shetland, it is reasonable to assume that the beaks were from L. forbesii. Identification of the stomach contents in the majority of predatory fish and marine mammals is at the level of the genus Loligo or family Loliginidae and, consequently, although in many cases the predators probably eat L. forbesii, we cannot rule out predation on L. vulgaris. Confusion with predation on Alloteuthis spp. is less likely because the beaks of this genus are distinguishable (see Clarke, 1986). Loliginid beaks have been reported from the stomachs of pygmy sperm whale (Kogia breviceps), northern bottlenose whale (Hyperoodon ampulatus), common dolphin (Delphinus delphis), striped dolphin (Stenella coeruleoalba), bottlenose dolphin (Tursiops truncatus), Atlantic white-sided dolphin (Laganorhynchus acutus), killer whale (Orcinus orca), long-finned pilot whale (Globicephala melas), and Risso’s dolphin (Grampus griseus) (as seen in, for example, De Pierrepont et al., 2005; Santos et al., 2014). None of these predators were considered to be a major cause for mortality of Loligo species. In some cases, the geographic location from which samples were obtained makes it reasonably certain that the beaks were from L. forbesii (MacLeod et al., 2014). Pierce and Santos (1996) note that the species is also eaten by grey seals (Halichoerus grypus) and harbour seals (Phoca vitulina) and suggested that marine mammals could consume a greater amount than is taken by fisheries in Scotland. Cannibalism is known for the species, and it is also preyed upon by its congener L. vulgaris (Guerra and Rocha, 1994). Table 12.4. Known predators of Loligo forbesii in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopoda European squid (Loligo vulgaris) Guerra and Rocha (1994) 152 | ICES Cooperative Research Report No. 325 Chondrich- Blonde ray (Raja brachyura) Farias et al. (2006) Atlantic cod (Gadus morhua) Daly et al. (2001), Magnussen (2011) Atlantic lizardfish (Synodus Soares et al. (2003) thyes Osteichthyes saurus) Monkfish (Lophius piscatorius) Daly et al. (2001) Swordfish (Xiphias gladius) Salman (2004) Aves Great skua (Catharacta skua) Furness (1994) Pinnepedia Grey seal (Halichoerus grypus) Pierce et al. (1991a) Harbour seal (Phoca vitulina) Brown and Pierce (1998) Harbour porpoise (Phocoena Rogan and Berrow (1996), Santos et phocoena) al. (2005b) Risso's dolphin (Grampus griseus) Bearzi et al. (2011) Sperm whale (Physeter macro- Clarke and Pascoe (1997), Santos et cephalus) al. (1999*, 2001b) Striped dolphin (Stenella co- Würtz and Marrale (1993) Cetacea eruleoalba) *This was a single beak 12.7 Fisheries Loligo forbesii is one of the two loliginid species of significant commercial importance in the Northeast Atlantic. As noted in the account for L. vulgaris, landings are not routinely recorded by species, and both FAO and ICES report figures for long-finned squid (Loliginidae); sometimes even this level of taxonomic disaggregation is unavailable. Scotland is probably the only reporting unit with significant catches for which it can be safely assumed that most long-finned squid landings reported to ICES are L. forbesii. Between 2000 and 2010, landings from the northern North Sea fluctuated from ca. 350 t in 2001 to 21 000 t in 2010, with a further 70–450 t arising from the west coast (ICES Division VIa). Interestingly, landings from the offshore ICES Division VIb, which includes Rockall, rose from <100 t annually to >700 t in 2008, possibly indicating the reemergence of the Rockall fishery, which last generated substantial landings in the 1980s (see below). Although landings dipped to slightly over 200 t in 2009, they increased to 700 t again in 2011 (ICES, 2012). Note that these trends in landings in Scotland do not follow the overall trends for loliginid landings in the European ICES Area which, over the same time-period, show a peak in 2003 (ICES, 2012). Although this trend should not be overinterpreted, it is likely that the two Loligo species show different abundance trajectories (see also Chen et al., 2006). Records of landings in Scotland go back to the early 20 th century (Thomas, 1969), although the quantities landed remained small for several decades, and dropped to a few tens of tonnes during the two world wars. The species supported a directed fishery by Denmark and Sweden in the North Sea and Skagerrak in the years 1948–1953 (Arnold, 1979). The fishery in Scotland expanded in the mid-1950s, facilitated by the advent of deep-freeze facilities and exports to continental Europe, and targeted fishing from small boats emerged in the English Channel in the mid-1970s (Arnold, 1979). Since the rise and fall of the short-lived fishery for Todarodes sagittatus in Norway, L. forbesii has been the dominant squid species fished north of the English Channel. The seasonality of fishing is related to the seasonality of recruitment. Depending on the area, there are one or several associated pulses of recruitment. Two main pulses of recruitment have been reported in Scotland in April and November, though with small Cephalopod biology and fisheries in Europe: II. Species Accounts | 153 numbers of recruits present throughout most of the year (Lum-Kong et al., 1992; Boyle and Pierce, 1994; Pierce et al., 1994b; Collins et al., 1997, 1999). The April recruitment may represent summer spawners. Shifting seasonal patterns in historical fishery landing data for Scotland are consistent with the relative importance of summer and winter breeding seasons having fluctuated since the 1970s (Pierce et al., 2005). In northern Europe and beyond the coastal zone in southern Europe, L. forbesii is mainly taken as bycatch in demersal trawl fisheries (e.g. Pierce et al., 1994b). The importance of directed fishing may be limited by the wide fluctuations in abundance reported (Young et al., 2004; 2006b), and there also appear to have been historical shifts in distribution (e.g. a disappearance from the southern part of its range in Atlantic coastal waters for several years; Chen et al., 2006). In Scotland, some trawl landings originate from 480 km west of mainland Scotland around Rockall. Although fishing in the area is mainly targeted at whitefish (e.g. haddock), it appears that squid have been targeted when abundant. Catches of L. forbesii at Rockall are made mainly in July and August when only the smallest recruits are caught in coastal waters, so possibly representing exploitation of a different stock. Catches from Rockall were greatly reduced after the mid-1980s (Pierce et al., 1994b, 2005). A small directed trawl fishery for squid exists close inshore in the Moray Firth (North Sea, Scotland). This fishery is strongly seasonal (September–November) and usually involves only a few small trawlers between 10 and 17 m in length (Anon., 2000). In the mid-2000s the number of trawlers taking part in this fishery increased dramatically (Young et al., 2006b), but subsequently decreased again (Smith, 2011). In Portuguese and Galician waters, although official fishery statistics indicate that L. forbesii is mainly taken as a bycatch in the multispecies trawl fisheries, local artisanal fisheries employing handjigs also exist (Cunha and Moreno, 1994; Guerra et al., 1994; Rocha et al., 1994). Loligo forbesii is the only squid species of economic importance in the Azores, where it is fished by an artisanal fleet equipped with handlines and homemade jigs (Martins, 1982; Porteiro, 1994). There is also some jigging for the species in the English Channel (Hamabe et al., 1982). Investigation of morphometric variation throughout the range, coupled with the development of molecular markers for this species, suggests no significant separation of stocks throughout the range of its distribution on mainland coasts (Pierce et al., 1994d, e; Brierley et al., 1995; Collins et al., 1997, 1999; Shaw et al., 1999). There is, however, some evidence that animals from offshore, sampled around Rockall Bank west of the UK, may be distinct from the coastal population. Boyle and Ngoile (1993b) recorded morphometric differences between coastal and offshore squid, and Shaw et al. (1999) confirmed differences at the molecular level. In the Azores, the degree of morphometric and genetic difference suggests a highly isolated population based on an introductory event up to 1 million years ago (Shaw et al., 1999); the differences may be sufficient to justify recognition of a separate subspecies (Brierley et al., 1995). 12.8 Future research, needs, and outlook It is a common theme across all the exploited cephalopod species in European waters, but there is a clear and urgent need for routine identification of all landed cephalopods to species level. This is of particular concern in L. forbesii and L. vulgaris which, despite their superficial morphological similarity, have different habitat preferences and show distinct population trends (see Chen et al., 2006); therefore, assessment of the combined stocks would not be meaningful. Robin and Boucaud-Camou (1995) have shown that 154 | ICES Cooperative Research Report No. 325 market sampling could be used to quantify monthly changes in proportions of the two Loligo species landed along the French coast of the English Channel. There is a need to develop routine stock assessment for loliginid squid fisheries in Europe, along with appropriate management measures. If squid fishing is to expand, there will need to be more use of selective gear such as jigs, because the bycatch of finfish could be an issue where there is targeted trawling. In the UK, trials to test jigs for squid catching in the 1970s and 1980s were largely unsuccessful (see Pierce et al., 1994b), but it seems likely that this was, to a large extent, a consequence of poor knowledge of squid distribution and abundance fluctuations. More studies are also needed on the artisanal fisheries that harvest this species (among other loliginids) in coastal waters of southern Europe. In the Azores, depredation by Risso’s dolphins (Grampus griseus) has the potential to cause significant economic losses in the jig fishery. Such issues would need to be managed if jig fishing for squid were to expand into the larger-scale fishing sectors. Finally, much more could be learned about the distribution and migration of this species, given access to logbook and VMS position data that are potentially available for a large proportion of the European fishing fleet. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Alloteuthis subulata European common squid | 155 156 | 13 ICES Cooperative Research Report No. 325 Alloteuthis subulata (Lamarck, 1798) Lee C. Hastie, Graham J. Pierce, Ana Moreno, Patrizia Jereb, Evgenia Lefkaditou, Daniel Oesterwind, Manuel Garcia Tasende, Uwe Piatkowski, and A. Louise Allcock Common names Casseron commun (France), calamaretto (Italy), lula-bicuda-comprida (Portugal), calamarín picudo (Spain), European common squid (UK) (Figure 13.1). Synonyms Loligo subulata Lamarck, 1798, Sepia subulata: Bosc (1802), Sepiola subulata: Gervais and Beneden (1838). 13.1 Geographic distribution The European common squid, Alloteuthis subulata (Lamarck, 1798) is found in the Northeast Atlantic from ca. 60°N to 20°N and has been reported from several areas of the Mediterranean (Figure 13.2), although it is considered to be absent from the Sea of Marmara and the easternmost parts (Jereb et al., 2010). In the Northeast Atlantic, the species is particularly abundant in Irish waters (Massy, 1928; Lordan et al., 1995; Nyegard, 2001) and the English Channel (Rodhouse et al., 1988). It is common in the North Sea (De Heij and Baayen, 2005; Oesterwind et al., 2010), from northern Scottish waters (Stephen, 1944) and the southwest coast of Norway (Grieg, 1933) to the English Channel, and is considered the dominant cephalopod species in the southern North Sea (De Heij and Baayen, 1999). It is present in the Kattegat, where it is regularly caught in Swedish waters (Hornbörg, 2005), Figure 13.1. Alloteuthis subulata. and it enters the western Baltic Sea occasionally Dorsal view. From Guerra (1992). (Herrmann et al., 2001). Distributed along the French, Spanish, and Portuguese coasts, it extends south onto the Sahara Bank, and, according to Adam (1952), to Rio de Oro waters (Cape Blanc, southwestern Sahara, see also Balguerias et al., 2000). Alloteuthis subulata has been found in the western and central Mediterranean (Mangold-Wirz, 1963a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Relini et al., 2002; Cuccu et al., 2003a) and in the eastern Ionian Sea (Kaspiris and Tsiambaos, 1986; Lefkaditou et al., 2012). A few records of the species from the northern Aegean Sea exist from trawl surveys (D’Onghia et al., 1996; Salman et al., 1997), but these have not been confirmed by the most recent investigations (Lefkaditou et al., 2012), so remain questionable. Although Zuev and Nesis (1971) refer to the presence of A. subulata in the Sea of Marmara, it has not been recorded during recent studies in that sea (Katağan et al., 1993; Ünsal et al., 1999). Also, old records of this species from the Levantine basin remain questionable (see Remarks). Cephalopod biology and fisheries in Europe: II. Species Accounts | 157 Figure 13.2. Alloteuthis subulata. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 13.2 Taxonomy Loliginid squids have been under constant systematic revision for many years. Two species placed in the genus Alloteuthis Wülker, 1920, Alloteuthis subulata and A. media, have been the object of numerous morphological and molecular studies in recent years (see Remarks for details). Results confirmed that two species exist in European waters, but, given that the type specimen of subulata is not extant and the whereabouts of the type specimen of media has not been confirmed, taxonomic issues abound (Allcock, 2010). Clearly, further studies are required to help define the whole species complex. Until the taxonomic situation with A. media and A. subulata is resolved, we elect to retain them here as separate entities (see also Jereb et al., 2010). 13.2.1 Systematics Coleoidea – Decapodiformes – Myopsida – Loliginidae – Alloteuthis. 13.2.2 Type locality Mediterranean Sea. 13.2.3 Type repository Assumed to have originally been Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. However, type specimen has not been found here [fide Lu et al. (1995)]. 158 | 13.3 ICES Cooperative Research Report No. 325 Diagnosis 13.3.1 Paralarvae Paralarvae are not described, but embryonic statoliths are documented (Morris, 1993). The young stages are visually almost indistinguishable from Loligo spp. (Grimpe, 1925; Hanlon et al., 1992). However, compared with Loligo forbesii, hatchlings of A. subulata have a different chromatophore arrangement, with more yellow chromatophores (Degner, 1925; Hanlon et al., 1992). Sizes of hatchlings are given as 1.5–2.2 mm ML by Jereb and Roper (2010), with most guides citing a size of ca. 2 mm. However, Yau (1994) indicated mean hatching size to be 2.0–2.8 mm. This is smaller than the typical hatching size for L. forbesii of ca. 4.5 mm (Boletzky, 1987b; Hanlon et al., 1989), although Gowland (2002) quotes 3 mm for hatching size in L. forbesii, suggesting some potential for confusion. 13.3.2 Juveniles and adults Juvenile A. subulata have a bullet-shaped body, with well-developed, paddle-shaped, terminal fins coming to a simple point at the apex. This apex develops into a tail in the subadult stage (Yau, 1994). Although young stages are similar to those of Loligo spp., the chromatophore arrangement still differs, with more yellow chromatophores than in L. forbesii (Degner, 1925; Hanlon et al., 1992; Yau, 1994). Like all squid in the family Loliginidae, adult A. subulata are muscular, with elongated mantles and clearly-defined fins (Nesis, 1982/1987). The fins are situated on the posterior half of the mantle, reaching its posterior end. The arms have two series of suckers, and the tentacles widen into clubs at the ends with four series of suckers. Members of the genus Alloteuthis can be separated from other genera of the family Loliginidae based on their small size as adults (although care must be taken to avoid confusion with young Loligo) and a mantle that is 6- to 15-fold longer than its width. The fins are ca. rhomboidal, longer than wide, and end far from the anterior edge of the mantle; they are convex on the anterior edge and attenuate posteriorly into a long, slender tail, which can be more than 50% of the mantle length in males. The fin width is >25% of the mantle length and the longest arm is 20–25% of the mantle length. The tentacles are considerably shorter than the head and mantle combined, with narrow clubs that have pairs of central suckers attached obliquely to the club axis at an angle of ca. 45° (Nesis, 1982/87). The tentacle club arrangement is similar in juveniles and adults, with median series of suckers three- to fourfold larger than marginal suckers (Yau, 1994). The left ventral arm (IV) is hectocotylized in mature males, with 6–8 pairs of normal suckers proximally followed by two longitudinal series of fine papillae distally (Yau, 1994). Within the genus Alloteuthis, A. subulata has traditionally been separated from other members of the genus (A. media and A. africana) based on the length of the tail and fins; a tail up to 20 mm long in females, and 50–60 mm long in males, and fins that are more that 50% of ML, are reported by Nesis (1982/1987). Recent studies, however, suggest that these characters offer a doubtful and unreliable tool for separating the species (Laptikhovsky et al., 2002, 2005; Anderson et al., 2008). First, these characters are evident only upon attainment of maturity (Laptikovsky et al., 2005). Second, the nature of morphometric sexual dimorphism differs between species; females grow larger in A. media, whereas males develop a longer mantle and tail in A. subulata and A. africana (Arkhipkin and Nekludova, 1993; Lefkaditou et al., 2012). According to Nesis (1982/1987), Laptikovsky et al. (2002), and Anderson et al. (2008), the relative size of club suckers (as described by Naef, 1921/1923) is informative for separating A. subulata and A. media (the suckers are smaller in A. subulata). In addition, Lefkaditou et al. (2012) showed that, using the length of the anterior part of the mantle, i.e. mantle length (ML) Cephalopod biology and fisheries in Europe: II. Species Accounts | 159 minus fin length (FL), as a reference length, the relative arm length (much shorter in A. subulata) can be used to distinguish this species from A. media (see the A. media account in the present volume for additional details). In addition, Muus (1963) indicated that at 30–50 mm ML, A. subulata has a shorter tentacular club than A. media (club no more than 11 mm compared with at least 12 mm). According to Roper et al. (1984), maximum ML is ca. 200 mm. Hastie et al. (2009b) give maximum ML as 215 mm in males and 150 mm in females, whereas Jereb et al. (2010) reported maximum ML as 184 mm for males and 140 mm for females; in both cases, values are based on examination of available literature. Regional studies give various maximum lengths (unless otherwise stated, these refer to males), but differences may reflect relatively limited sampling periods or areas. Moreno (1995) reports a maximum size in Portuguese waters of 183 mm ML. The largest individuals sampled in the English Channel during 1985 and 1986 measured ca. 160 mm ML (Rodhouse et al., 1988). Arkhipkin and Nekludova (1993) mention individuals up to 180 mm ML off West Africa. Nyegaard (2001) reported mean sizes in the Irish Sea as 55–87 mm ML for males and 58–108 mm for females, depending on the month. In a more recent study (G. Stowasser, pers. comm.), the species was sampled in three areas, and size ranges for mature specimens were 80–120 mm in females and 90–160 mm in males in the Irish Sea, 60–90 mm in females and 70–120 mm in males in the northern North Sea, and 60– 100 mm in females and 50–120 mm in males in the German Bight. In another North Sea study, maximum length of females in winter was 113 mm and that of males was 151 mm, but in summer, both sexes were larger on average (females, maximum 117 mm; males, maximum 160 mm) (Oesterwind et al., 2010). 13.4 Remarks Although it appears to be safe to conclude that there are two distinct morphotypes of Alloteuthis in European waters, real doubts remain as to the true taxonomic affiliation of the animals we currently think of as A. subulata and A media. Assuming that there are two distinguishable European species, there is a strong likelihood that past misidentifications have resulted in mixing of information on both species. Laptikhovsky et al. (2002) suggested that A. subulata and A. media are intraspecific forms rather than true species, although the large degree of sympatry between the two types indicates that this is not simply a case of minor differences between allopatric populations. Anderson et al. (2008) supported a sister-species relationship between A. media and A. subulata. According to those authors, who analysed both morphometric and DNA sequence data from Alloteuthis specimens from several localities, central club sucker size can be used to separate A. media from A. subulata, but relative fin length, an easily diagnosable character often used to distinguish Alloteuthis species, appears to be of little taxonomic value. As type specimens of neither A. media nor A. subulata can be located, there are real nomenclatural issues. Anderson et al. (2008), considering morphometric and genetic characters, assigned three specimens from the Adriatic to A. subulata, but without recourse to type material, the validity of these assignations is impossible to verify. Further details of the issues are given in the Remarks section of the A. media account. As a consequence of the above-mentioned taxonomic issues, the exact geographic limits of the distributions of A. media and A. subulata remain uncertain. The remainder of this account assumes that the morphotypes we think of as representing the two species have been correctly assigned. However, it remains probable that there has been confusion over the years. Hence, Llewellyn (1984) comments that A. subulata was reported as Loligo media by Beauchamp (1912). 160 | ICES Cooperative Research Report No. 325 Old records of this species in the eastern Mediterranean, Sea of Marmara, and Levantine Basin (i.e. Gruvel, 1931; Ruby and Knudsen, 1972) remain questionable (see Lefkaditou et al., 2012, for additional details). Studies of morphometric characters and maturation, based on Alloteuthis samples collected from the Levant, Aegean, and Marmara seas, noting also the wide range of size at maturity for both females and males that might lead to species misidentification, suggested that the genus Alloteuthis is represented by a single taxonomic unit in the eastern Mediterranean, which should be A. media (Laptikhovsky et al., 2002; 2005). The mention of the presence of the species as Loligo subulata (Gruvel, 1931) in Syrian waters is also questionable (Lefkaditou et al., 2012) and probably refers to A. media. Two female A. subulata (one from off Haifa, the other from an unknown locality) are listed by Ruby and Knudsen (1972) for the waters off Israel, but the only other mention of Alloteuthis specimens from that area refers to A. media (Adam, 1966; one male). Therefore, the presence of A. subulata in the easternmost waters of the Mediterranean remains questionable. 13.5 Life history Alloteuthis subulata is a typical small, fast-growing, short-lived cephalopod. Its life cycle can be as short as 6 months (Arkhipkin and Nekudova, 1993) and possibly sometimes as long as 12 months, but there may be several spawning seasons, each probably associated with a different “microcohort”. 13.5.1 Egg and juvenile development Mature ova are reported to measure 1.55 mm (Hastie et al., 2009b). During spawning, gelatinous capsules 30–50 mm long and containing a number of eggs are usually attached to a solid substratum (Yau, 1994). Mantle length of A. subulata on hatching is reported to be 1.5–3.2 mm (Mangold-Wirz, 1963a; Yau, 1994; Jereb and Roper, 2010). Incubation time for eggs is 2–3 weeks at 15–18°C (Lipiński, 1985), but could be longer in cooler waters. Paralarvae and juveniles are planktonic at first, but shift to a nearbottom mode of life 15–30 d after they first appear in the plankton (Yau, 1994). Based on observations of an egg mass kept in an aquarium, Yau (1994) estimated the time of hatching in Scottish waters (North Atlantic) to be around May. 13.5.2 Growth and lifespan Males and females have similar length–weight relationships until ca. 70 mm ML, when females become relatively heavier than males of a similar length, as reflected in the higher slope coefficients in females (Table 13.1). However, males generally achieve larger body sizes overall (Rodhouse et al., 1988; Hastie et al., 2009b). Cephalopod biology and fisheries in Europe: II. Species Accounts | 161 Table 13.1. Alloteuthis subulata. Length–weight relationships in different geographic areas for females (F) and males (M). Original equations converted to W = aMLb where W is body mass (g) and ML is dorsal mantle length (cm). From Hastie et al. (2009b). Region a b Sex Irish Sea 0.291 1.39 M Irish Sea 0.150 1.84 F North Sea 0.184 1.59 M North Sea 0.160 1.77 F Portugal 0.420 1.20 M Portugal 0.167 1.83 F As in other loliginids, length frequency data for the North Sea suggest the existence of several microcohorts, representing animals with different growth rates and/or hatching times (and potentially also mapping onto different spawning periods), which might be attributable to different spatial variation in water temperatures within the species range (Oesterwind et al., 2010). Oesterwind et al. (2010) described five cohorts for males and four cohorts for females in summer. There were two cohorts of males and females in the entire North Sea in winter. Differences between summer and winter length frequency distributions presumably reflect the annual nature of the life cycle. Growth increments in the statoliths are thought to be deposited daily (Lipiński 1985, 1986; Morris 1993). This provides growth estimates of between 0.03 and 0.1 cm d –1. On the West African shelf, absolute growth rates ranged between 0.5 and 1.0 mm d–1 in length and from ca. 0.03 to 0.06 g d –1 in weight. Instantaneous relative daily growth rates fell from ca. 2.2% ML d–1 and 3.5% BW d–1 at 90 d of age to ca. 0.8% ML d–1 and 0.5% BW d–1 at 210 d (Arkhipkin and Nekludova, 1993; see their Figures 8 and 9). Rodhouse et al. (1988) indicate a lifespan of ca. 12 months in northern temperate waters, but Arkhipkin and Nekudova (1993) proposed a lifespan of 6 months for the population off Northwest Africa, based on statolith analysis. 13.5.3 Maturation and reproduction Hastie et al. (2009b) reported seasonal variation in sex ratio, with a slight overall preponderance of males (M:F = 1.04–1.14 depending on region), although females were relatively more abundant in spring in Portugal (M:F = 0.76) and during summer in the North Sea and Irish Sea (M:F = 0.76 and 0.78, respectively). Progressive maturation in A. subulata occurs from winter to late spring or summer, beginning when the animals reach 30–40 mm ML. Sexual maturity can be reached at 40–50 mm ML in both sexes (North Sea: 44 mm ± 9 mm in females; 43 mm ± 10 mm in males). Some 50% of females are mature at a length of 75–80 mm, and MLm50% for males is 70–75 mm. However, the length of mature animals varies considerably in both sexes, with mature males having a wider range of sizes (39–183 mm) than mature females (54–104 mm) (Moreno, 1995). Males mature slightly earlier than females, and the majority of the population reaches maturity by late spring (Portugal) or summer (English Channel and North Sea) (Rodhouse et al., 1988; Moreno, 1990, 1995; Oesterwind et al., 2010). Relatively large immature males (120 mm ML) and females (75 mm ML) are sometimes caught in Portuguese waters in winter, indicating that there may be variations in the life cycle described above (Moreno, 1995). 162 | ICES Cooperative Research Report No. 325 Within any year, there may be several more or less distinct spawning periods. For example, in the English Channel, there are three spawning groups of females that spawn in spring, summer, and autumn, respectively1, with young individuals being recruited to the population twice during the year, in spring and summer. In the Irish Sea, spawning takes place in spring and summer, with a possible minor spawning period in autumn (Nyegaard, 2001). In the North Sea, spawning is in June–July, with hatchlings appearing in plankton samples towards the end of July (Yau, 1994). Spawning probably takes place earlier off the west coast of Scotland than in the North Sea (Yau, 1994). The polymodal egg size frequency distribution seen in ovaries might be explained by batch spawning (Hastie et al. (2009b). Based on examination of 11 female A. subulata ranging in size from 8 to 12.1 cm ML, the average number of oocytes present (potential fecundity) is 5705 (range = 1234– 18 770). This contrasts with ”batch counts” that indicate an average of 148 eggs laid in any one session and that actual fecundity is between 400 and 1500 eggs (Nyegaard, 2001). Perhaps each female lays a number of batches of eggs throughout her lifetime, possibly as many as 40 batches. Whether this maximum number of batches is finally produced may depend on female condition and mortality during the spawning season (Nyegaard, 2001). 13.6 Biological distribution The biology and ecology of this species were reviewed in Hastie et al. (2009a), and reproductive biology was described by Hastie et al. (2009b); these papers may be consulted for further details. 13.6.1 Habitat Alloteuthis subulata is a near-bottom species that lives in shelf waters, particularly in the North Sea (Grimpe, 1925; Steimer, 1993), Kattegat, and western Baltic Sea (e.g. Jaeckel, 1937; Herrmann et al., 2001; Hornbörg, 2005). In UK waters, the species is abundant in the English Channel (Rodhouse et al., 1988) and the Irish Sea (Nyegaard, 2001). It is found from the coast out to ca. 500 m depth (Guerra, 1992), although mainly between 20 and 120 m, and captures below 300 m are sporadic (Roper et al., 1984; Jereb et al., 2010). In Portuguese waters, it is often abundant at 20–200 m (Moreno, 1990, 1995). In the western Mediterranean, it is primarily recorded at depths of 34–278 m (González and Sánchez, 2002). 13.6.2 Migrations In some parts of its range, A. subulata is present year-round (e.g. in the English Channel; Rodhouse et al., 1988), but in other parts, it is thought to be migratory. For example, in the North Sea, juveniles are reported to leave the area at an age of ca. 3 months in November and return the following spring at a size of ca. 5 cm. Both males and females move inshore in early summer (Yau, 1994). However, studies along eastern North Sea coasts (and recent trawling surveys) suggest that juvenile A. subulata migrate from the spawning grounds in the southeast to the deeper (and, in winter, relatively warmer) waters in the central parts during late autumn/winter, perhaps as a response to cooling. 1 Such apparently contradictory life-cycle features have also been noted in other loliginids such as L. forbesii, with various explanations being proposed for the mismatch of spawning and recruitment periods. Cephalopod biology and fisheries in Europe: II. Species Accounts | 163 In spring, as the waters warm, the young adults return from the Danish coast to shallow waters off the Belgian and southeast British coasts to spawn (De Heij and Baayen, 1999, 2005; Oesterwind et al., 2010). 13.7 Trophic ecology 13.7.1 Prey The main prey species of A. subulata in the Irish Sea are reported to be clupeid fish and crustaceans (Nyegaard, 2001). In the North Sea, fish prey consists mainly of Gobiidae, but Clupeidae, Gadidae, and sandeels (Ammodytidae) are also common (Table 13.2). Diet composition varies significantly in relation to body size (ML). Small A. subulata feed mainly on crustaceans, but fish remains are increasingly commonly found in the stomachs of larger individuals. Larger A. subulata also eat larger prey (Oesterwind, 2011). Alloteuthis subulata feeds in the pelagic zone rather than close to bottom (Hastie et al. 2009a). The estimated maximum length of fish prey is ca. 7 cm in the North Sea (Oesterwind, 2011). Llewellyn (1984) observed the feeding behaviour of the species in aquaria, noting that squid fed readily on “prawns, shrimps, mysids and gobies” introduced into the tanks, although such prey were ignored if they were on the bottom of the tank. “Food capture was effected by the squid darting forward in a straight line from as far as ca. 20 cm from the prey; the prey was held between the arms and tentacles and then usually swallowed within a few seconds.” Table 13.2. Prey composition of Alloteuthis subulata, as known from studies in the Northeast Atlantic (compiled from Lipiński, 19851; Nyegard, 20012; Hastie et al., 2009a3, Oesterwind, 20114, pers. comm.5). Taxon Species Osteichthyes Am- Ammodytes tobianus (sandeel)3, indet.4 modytidae Clu- Sprattus sprattus (European sprat)3, indet.2,4 peidae Ga- indet.4 didae Gobi- Pomatoschistus minutus (sand goby)1,5, Crystallogobius linearis (crystal goby)5, idae Gymnammodytes semisquamatus (smooth sandeel)5, Aphia minuta (transparent goby)5 Polychaeta indet.4 Crustacea Mysida indet.1, indet.2,4 Cephalop- indet. squids1 oda 13.7.2 Predators Alloteuthis subulata is an important item in the diet of many predatory fish in the Northeast Atlantic, North Sea, and adjacent waters, including cod, hake, whiting, ling, tuna, sharks, halibut, wolfish, and plaice (Zuev and Nesis, 1971; Hislop et al., 1991; Daly et 164 | ICES Cooperative Research Report No. 325 al., 2001; Velasco et al., 2001). It is the most commonly recorded cephalopod species in stomach contents of demersal fish in UK waters (Hislop et al., 1991; Daly et al., 2001). Several marine mammals and larger cephalopod species are also recorded as feeding on A. subulata (Table 13.3; see also Hastie et al., 2009a). In some studies, Alloteuthis spp. was recorded; for example, the genus was found in 6 of 10 stomachs of striped dolphin sampled in Galicia during the years 1990–2009 (Sollmann, 2011). Table 13.3. Known predators of Alloteuthis subulata in the Mediterranean Sea and Northeast Atlantic. Taxon Species Cephalopoda European squid (Loligo vulgaris) References Pierce et al. (1994a), Rocha et al. (1994) Veined squid (Loligo forbesii) Pierce et al. (1994a), Rocha et al. (1994) Chondrich- Blonde ray (Raja brachyuran) Farias et al. (2006) Milk shark (Rhizoprionodon Patokina and Litvinov (2005) thyes acutus) Osteichthyes Spotted ray (Raja montagui) Farias et al. (2006) Thornback ray (Raja clavata) Farias et al. (2006) Albacore (Thunnus alalunga) Consoli et al. (2008), Romeo et al. (2012) Brill (Scophthalmus rhombus) Vinagre et al. (2011) European hake (Merluccius mer- Daly et al. (2001) luccius) Red gurnard (Chelidonichthys cu- Lopez-Lopez et al. (2011) culus) Tub gurnard (Chelidonichthys lu- Lopez-Lopez et al. (2011) cerna) Cetacea Whiting (Merlangius merlangus) Hislop et al. (1991), Pedersen (1999) Bottlenose dolphin (Tursiops trun- Santos et al. (2001b, 2005a) catus) Common dolphin (Delphinus del- González et al. 1994a), Meynier phis) (2004), Santos et al. (2013) Striped dolphin (Stenella coerule- Sollmann (2011) oalba) Harbour porpoise (Phocoena Börjesson et al. (2003), Santos et al. phocoena) (2005b), Jansen et al. (2013) Northern bottlenose whale (Hy- Santos et al. (2001c) peroodon ampullatus) Aves 13.8 Puffin (Fratercula arctica) Hislop and Harris (1985) Other aspects of biology and ecology 13.8.1 Parasites According to Zuev and Nesis (1971), the trematode (monogenean) Isancistrum loliginis has been noted on gills (it was originally described by Beauchamp, 1912) and the nematode Filaria loliginis in the mantle cavity and ovary. Llewellyn (1984) described a new Cephalopod biology and fisheries in Europe: II. Species Accounts | 165 monogenean species, Isancistrum subulatae, mainly on the arms and tentacles of A. subulata (and probably never on the gills). González et al. (2003) recorded the copepod Pennella sp. on a range of cephalopods in Galicia, including A. subulata. 13.8.2 Behaviour Llewellyn (1984) recorded the shoaling behaviour of Alloteuthis in aquaria, noting that under bright artificial light: “the squid frequently swam in loosely-regimented shoals of ca. 5–10 individuals with an interval between individuals of ca. 10–20 cm, and with each shoal being confined usually to a volume of ca. 40 × 40 × 40 cm. Occasionally individuals strayed from the shoal, but they very soon rejoined it“. In darkness, the squid scattered, but they reassembled into a shoal within a few minutes of the light being turned on. In addition, mating was observed on one occasion; two squid “were seen to copulate by frontal approach and mutual intermingling of the arms and tentacles... The coupling lasted for... ca. 20 seconds”. 13.9 Fisheries Alloteuthis subulata is not currently the main target of any directed fishery and is of relatively low commercial value because of its small size (Moreno, 1995). However, Alloteuthis spp. are landed and marketed as a secondary target or bycatch in Spain, Portugal, and Italy. As commented elsewhere, landings of loliginid squids in Europe are usually not identified to species, and Alloteuthis spp. are probably also frequently landed (unrecognized) in commercial trawl catches of Loligo spp. throughout their ranges. During certain years, both A. subulata and A. media can be important components of Portuguese cephalopod catches, although they do not appear in commercial fishery statistics (Moreno, 1995). Both Alloteuthis species are also landed in Galicia (northwestern Spain). In 2010, 13 t of Alloteuthis were landed in Galicia, but most originated from distant fishing grounds (data from www.pescadegalicia.com). Landings from Galician fishery grounds (900 kg) were recorded, mainly in summer and autumn, presumably as a secondary target species (after Loligo vulgaris) in the boliche (boat seine net) fishery (Tasende et al., 2005) inside the Galician rías (500 kg, M. G. Tasende, pers. comm.). The remainder was caught with trawl (200 kg) or purse-seine (200 kg) in grounds outside the rías. Alloteuthis subulata may also be caught and misidentified as juvenile L. forbesii in directed fisheries for that species (e.g. in the Moray Firth, Scotland). In some southern European countries, a minimum landing size (MLS) is set for Loligo spp. (for example, 10 cm in Portugal; Fonseca et al., 2008) and in Galicia, there is also a MLS (6 cm) for Alloteuthis (Tasende et al., 2005). In general, given the intraspecific variability in growth patterns in loliginids, it is arguably difficult to set a meaningful MLS. In addition, in the future, it may be useful to consider protecting spawning areas. There is currently no information on whether A. subulata is a single, continuous, mixed population or is divided into a number of smaller populations with limited gene flow between them. However, as previously noted, larger taxonomic issues remain unresolved. 13.10 Future research, needs, and outlook Despite being one of the more common squid species in European waters, relatively little is known about A. subulata. This is probably because it is currently of little commercial fishery interest in most of Europe. However, if this situation changes, it will be 166 | ICES Cooperative Research Report No. 325 important to increase current knowledge of the biology of this species to allow adequate management procedures to be introduced. In addition, it will be necessary to distinguish Alloteuthis species routinely within landings data for loliginid squid. As noted above, the taxonomy of the genus Alloteuthis remains unresolved, and further work is urgently needed to confirm which Alloteuthis species are actually present and their distributions in European waters. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Alloteuthis media Mid-sized squid | 167 168 | 14 ICES Cooperative Research Report No. 325 Alloteuthis media (Linnaeus, 1758) Evgenia Lefkaditou, Cleopatra Alidromiti, Lee C. Hastie, Graham J. Pierce, A. Louise Allcock, and Patrizia Jereb Common names Casseron bambou (France), Καλαμαράκι [kalamaraki] (Greece), calamaretto comune (Italy), lulabicuda-curta (Portugal), calamarin menor (Spain), midsize squid (UK) (Figure 14.1). Synonyms Sepia media Linnaeus, 1758, Loligo parva Leach, 1817, Loligo subulata: Delle Chiaje (1831), Loligo marmorae Verany, 1837, Loligo urceolatus Risso, 1854, Loligo media: Jeffreys (1869), Acroteuthis media: Naef (1916). 14.1 Geographic distribution The midsize squid, Alloteuthis media (Linnaeus, 1758), is reported in the Northeast Atlantic and Mediterranean (Nesis, 1982/1987; Roper et al., 1984; Guerra, 1992; Jereb et al., 2010; Figure 14.2), but the limits of its distribution range in the Northeast AtFigure 14.1. Alloteuthis media. lantic are not well documented and remain un- Dorsal view. From Guerra (1992). clear, partly because of the difficulties in correctly identifying Alloteuthis species using morphometric characters only (see Remarks); hence, confusion exists in some of the old records of both species. Alloteuthis media is considered “rare” in the North Sea, but was specifically mentioned by Grimpe (1925) in the waters of the Helgoland archipelago (54°11’N 7°53’E) and reported to be present in the southern North Sea “only in small numbers in summer” by Zuev and Nesis (1971). It was not included in the cephalopods of Scottish waters by Stephen (1944) nor mentioned by Grieg (1933) for the waters of the west coast of Norway. Records by Russell (1922) in Scottish waters probably refer to A. subulata, as do the records of Massy (1909) along the Irish coasts (Massy, 1928). The presence of the species was mentioned in the Irish Sea by Moore (1937; Isle of Man) in Stephen (1944) and Zuev and Nesis (1971). Alloteuthis media is found in the English Channel, according to Stephen (1944), Zuev and Nesis (1971), and, more recently, Anderson et al. (2008). It is particularly abundant off the western Iberian coasts (Coelho and Borges, 1982; Moreno, 1990) and was also reported as abundant on the Sahara Bank (in the area between Cape Blanc, 21°N, and Cape Bojador, 26°N; Balguerias et al., 2000). Alloteuthis media is abundant and widely distributed throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), and it is found in the western part of the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999) (see Remarks). Cephalopod biology and fisheries in Europe: II. Species Accounts | 169 Figure 14.2. Alloteuthis media. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 14.2 Taxonomy As further discussed in the Remarks section below, the two species placed in the genus Alloteuthis (Wülker, 1920) have been the subject of numerous morphological and molecular studies in recent years. Results have confirmed that two species exist in European waters, but the type specimen of subulata is not extant, and the whereabouts of the type specimen of media has not been confirmed (Allcock, 2010). Further studies are required, but until the taxonomic situation with A. media and A. subulata is resolved, we elect to retain them here as separate entities (see also Jereb et al., 2010). 14.2.1 Systematics Coleoidea – Decapodiformes – Myopsida – Loliginidae –Alloteuthis. 14.2.2 Type locality “Pelago” (Linnaeus, 1758) – literally “the sea”. 14.2.3 Type repository Unknown. The original description cites Rondelet (1554), which has a figure and detailed description. The Linnean Society of London was tentatively proposed as the repository of that specimen by Sweeney and Roper (1998), but enquiries to the Linnean Society suggest that no type is held in that repository (A. L. Allcock, pers. comm.). 170 | 14.3 ICES Cooperative Research Report No. 325 Diagnosis 14.3.1 Paralarvae The mantle length (ML) of hatchlings is 2.8 mm (Zuev and Nesis, 1971). A detailed description of A. media paralarvae is not yet available, and according to Sweeney et al. (1992), they are nearly indistinguishable from Loligo spp. 14.3.2 Juveniles and adults Alloteuthis media is a small member of the Loliginidae, not exceeding 13.2 cm ML (Laptikhovsky et al., 2002). There is morphometric sexual dimorphism, with females attaining larger size than males (Katsanevakis et al., 2008; Alidromiti et al., 2009). Similar to A. subulata, it has a narrow elongated mantle, with its posterior ending in a narrow, pointed tail, and the heart-shaped fins, with their lateral angles rounded, extending posteriorly along the tail. Very large and small chromatophores alternate on the mantle. When the length of the anterior part of the mantle (from the upper edge of the fins to the mantle opening) is used as a reference length, the arm length index ranges between 81 and 167% for A. media and 25 and 52% for A. subulata (Lefkaditou et al., 2012). For individuals of equal size, the tentacular club of A. media is 50–75% longer and 50% broader than that of A. subulata (Naef, 1921/1923; Zuev and Nesis, 1971). According to Muus (1963), in animals 30–50 mm ML, the tentacular club of A. media is at least 12 mm long as opposed to no more than 11 mm in A. subulata. The suckers of both arms and tentacles in A. media are larger than in A. subulata. Males lack the very long tails seen in A. subulata. On the hectocotylus, the apical suckers are larger, coarser, and fewer, whereas the median row in the proximal part has only 10–12 suckers. The beaks of A. media are transparent, with darkening limited to around the rostral tip in both the upper and lower mandibles (Figure 14.3). Pigmentation does not seem to be related to maturation (Mangold and Fioroni, 1966). The crest length is almost double the hood length, and the jaw angle is approximately a right angle in both mandibles. The hood and crest of the upper beak are considerably larger, reaching double the size of those in the lower beak (Mangold and Fioroni, 1966). Figure 14.3. Alloteuthis media. Lower beak (left) and upper beak (right) of a female (78 mm ML), from the Aegean Sea. Photo: Evgenia Lefkaditou. 14.4 Remarks While it appears to be safe to conclude that there are two distinct morphotypes of Alloteuthis in European waters, real doubts remain as to the true taxonomic affiliation of the animals we currently think of as A. subulata and A media, and (assuming that there Cephalopod biology and fisheries in Europe: II. Species Accounts | 171 are two distinguishable European species) there is a strong likelihood that past misidentifications have resulted in mixing of information on both species. As noted by Naef (1921/1923), the congeneric species A. media and A. subulata were not distinguished before his studies in 1912, so specimens described before that date probably included individuals of two species. However, in spite of Naef’s research and description, there has been continued confusion over the identification of the two species in the eastern Mediterranean, where the occurrence of A. media was considered questionable until the late 1980s (Mangold and Boletzky, 1987). The few individuals reported by Adam (1966) and, subsequently, by Ruby and Knudsen (1972) in the Levant basin were considered as possibly Loligo juveniles or A. subulata. Since the early 1990s, the occurrence and distribution of A. media in the Aegean Sea has been confirmed by research cruises (Katağan and Kocatas, 1990; D’Onghia et al., 1992, 1996; Salman et al., 1997; Lefkaditou et al. 2004). The species was first mentioned as present in the Sea of Marmara by Digby (1949), although more extensive trawl surveys in the1990s have shown that its distribution is limited to the southwest part of the Sea of Marmara, reflecting the species’ tolerance of a moderately brackish environment, but intolerance of waters with low levels of dissolved oxygen, such as those in the eastern part of the Sea of Marmara (Katağan et al., 1993; Ünsal et al., 1999). Morphometric studies on hundreds of Alloteuthis specimens collected from the Levant and Aegean seas suggested that the genus Alloteuthis is represented by a single taxonomic unit in the eastern Mediterranean, which should be A. media (Laptikhovsky et al., 2002, 2005). Analyses of DNA sequence data from Alloteuthis specimens collected from different subareas of the Mediterranean Sea indicated two distinct clades, confirming that two species exist (Anderson et al., 2008). Based on the description of the club by Naef (1921/1923), Anderson et al. (2008) considered that the clade extending throughout the eastern (Aegean Sea) and western (Catalan Sea) Mediterranean and several areas of the Northeast Atlantic corresponded to A. media. Those authors referred the clade sampled only from the Adriatic Sea (i.e. three specimens only) to A. subulata, which is also believed to live in the Ionian Sea (Lefkaditou et al., 2012). Despite following the morphological diagnostic characters used by Naef (1921/1923), Anderson et al. (2008) obtained conflicting results, because Naef considered A. subulata, with its smaller club suckers, to extend throughout the Atlantic (including the North Sea) and Mediterranean, and A. media, with its larger club suckers, to have a restricted distribution in the Mediterranean. Without recourse to type material, assigning names to morphotypes is extremely difficult. As noted above, the type of A. media appears not to be held at the Linnean Society. Linnaeus may not have deposited a specimen, because he refers to the drawing in Rondelet (1554). The type of A. subulata is presumed lost, because it could not be located at the Muséum National d'Histoire Naturelle in Paris (fide Lu et al., 1995). 14.5 Life history The lifespan of A. media is probably 9–11 months. Depending on the region, spawning may take place year–round, or there may be an extended spawning season. 14.5.1 Egg and juvenile development The eggs are shed in several batches and are encapsulated in rather short gelatinous strings laid on hard substrata such as stones and shells. An egg string consists of ca. 12 capsules containing 6–30 eggs each, giving a total of 200–300 eggs. The string resembles the string of A. subulata, but the capsules are broader with shorter stalks, and the string 172 | ICES Cooperative Research Report No. 325 itself is smaller. The eggs measure 1.0–1.5 mm along their major axis, and the egg capsules are 3–4 cm long. The eggs apparently mature in batches, but the duration of embryonic development is unknown (Zuev and Nesis, 1971). According to the description of the last embryonic stages of A. media by Capua et al. (2005), an external yolk sac is still present in embryos up to 2.4 mm ML, when rudimentary arms, funnel, and eyes are already clearly visible (Figure 14.4). B A C 1 cm H 1 mm 1 mm E 1 mm D 1 mm Figure 14.4. Alloteuthis media. Embryonic stages described by Capua et al. (2005) from an egg mass collected by trawl in the Ligurian sea, fixed in 4% formalin. (A) An egg string containing rows of eggs in a gelatinous matrix and showing the basal apparatus by which the string is connected to the substratum, (B) Detail of an egg at developmental stage 10–11, with blastoderm seen at the germinative pole, (C) embryonic form still enclosed into the egg (stage 23–24 ) with visible rudimentary arms (b), funnel (f), mantle (m) and external yolk sac (Se), (D) embryo (stage 29 of Arnold) with visible arms (a), eyes (e), funnel (f), digestive gland (g), ink sac (n), chromatophores (c), external (Se) and internal (Si) yolk sacs, (E) embryo (stage 30 of Arnold) showing brachial (Bc), dorsal (Cd) and ventral (Cv) chromatophores. Photos: Domenico Capua. 14.5.2 Growth and lifespan Alloteuthis media is a species of small size, with females reaching 120 mm ML and males 90 mm ML. The tail appears and grows during maturation (Laptikhovsky et al., 2002). Based on length frequency analyses, the longevity of A. media had been estimated to be ca. 1 year for males and 18 months for females, with a monthly growth rate decreasing from 7–8 mm in the first summer of life to 2–5 mm during the second year (Mangold- Cephalopod biology and fisheries in Europe: II. Species Accounts | 173 Wirz, 1963a; Zuev and Nesis, 1971; Auteri et al., 1987). However, recent direct age determination of A. media in the northwestern Aegean Sea, based on enumeration of daily increments in statoliths, has shown that the lifespan of females reaches up to 11 months, whereas the males can reach 9 months of age (Alidromiti et al., 2009). Growth rate (mantle length vs. age) is faster in females, which also reach a larger size. Best fit growth equations (ML in mm and age in days) according to Alidromiti et al. (2009) are as follows: Females: ML = 1.096 × Age0.7538 (ML = 1.096 × Age0.7538 r = 0.830, n = 73) Males: ML = 0.911 × Age0.7666 ML = 0.911 × Age0.7666 (r = 0.841, n = 46) In terms of length–weight relationships (see Table 14.1), females display higher values for the slope coefficient b (Belcari, 1999b). Table 14.1. Alloteuthis media. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Southern Portugal 0.099 2.22 F Moreno (1990) 0.185 1.79 M 0.106 2.07 F 0.143 2.01 M 0.244 1.76 All Northern Aegean Southeastern Aegean E. Lefkaditou, pers. comm. Akyol and Metin (2001) Research on age and growth of A. media in the northern Aegean Sea (Alidromiti, 2007) showed that growth rates of both sexes were faster in the eastern basin, which is characterized by relatively low temperature as a consequence of the cold and nutrient-rich Black Sea water inflow throughout the year. Hence, food availability, particularly the zooplankton biomass associated with Black Sea waters (Isari et al., 2007), is an important influence on A. media growth in this area. 14.5.3 Maturation and reproduction Individual maturity is reached over a wide range of mantle lengths, but mainly when the animals reach ca. half of the maximum mantle length. The MLm50% estimated for A. media in the Tyrrhenian and the Adriatic Seas is ca. 50 mm in males and 60 mm in females (Auteri et al., 1987; Soro and Piccinetti-Manfrin, 1989). Note, however, that the existence of multiple sizes at maturity in loliginid squids, especially males, can mean that such values are misleading. As in other cephalopods, it appears that there is a gradient of decreasing minimum mantle length at maturity from the western to the eastern basins of the Mediterranean. In the western basin, the smallest mature females measure 80 mm ML, and the smallest mature males 50 mm ML, relative to 37 mm ML for females and 32 mm ML for males in the eastern basin (Jereb et al., 2010). During the reproductive period, adults migrate to shallow water. Spawning in the Mediterranean is at depths of 10–100 m on sand, seagrass meadows, etc. The spawning season lasts from March to October in the western Mediterranean (Mangold-Wirz, 1963a), but is year-round in the central and eastern regions (Lo Bianco, 1909; Naef, 1921/1923; Laptikhovsky et al., 2002; Lefkaditou et al., 2007). In the North Sea, spawning takes place in June and July (Zuev and Nesis, 1971). 174 | ICES Cooperative Research Report No. 325 Oocyte maturation occurs in batches. The potential fecundity has been estimated at ca. 950–1400 eggs for the western Mediterranean, whereas typical values in the eastern Mediteranean (1500–2500) are higher. Ripe egg size in the eastern Mediterranean (1.5– 2.3 mm along the major axis) is somewhat larger than in females from the western area (1.4–1.6 mm) (Laptikhovsky et al., 2002). Larger females produce larger and heavier eggs. 14.6 Biological distribution 14.6.1 Habitat Alloteuthis media is among the most abundant demersal cephalopod species of the shelf community, as demonstrated by studies in the Gulf of Cádiz (Silva et al., 2011), the Iberian Mediterranean coast (González and Sánchez, 2002), the Tyrrhenian (Sánchez et al., 1998a), Adriatic and eastern Ionian seas (Ungaro et al., 1999; Krstulovic-Šifner et al., 2005), and the northern Aegean Sea (Lefkaditou, 2006); see also Katsanevakis et al. (2008). Generally, A. media inhabits a wide depth range from the coast down to 500– 600 m (Lefkaditou, 2007), although it is most common in water >150 m deep over sandy and muddy grounds. It is also found in brackish water (Ünsal et al., 1999). 14.6.2 Migrations Alloteuthis media undertakes seasonal migrations between offshore (in winter) and inshore (in spring) areas, where juveniles recruit mainly during summer and autumn (Mangold-Wirz, 1963a; Belcari, 1999b). Diel vertical migrations have also been described (Zuev and Nesis, 1971). 14.7 Trophic ecology 14.7.1 Prey Zuev and Nesis (1971) report that the diet of A. media from the Adriatic Sea consists of larvae and juveniles of fish, copepods, and euphausiids (Table 14.2). According to Guerra (1992), its diet off the Iberian Peninsula also includes molluscs. In the Aegean Sea, decapod crustaceans, mysids, and hydrozoans were identified among prey items (Vafidis et al., 2008). Table 14.2. Prey composition of Alloteuthis media, as known from studies in the eastern Mediterranean Sea (compiled from Zuev and Nesis, 19711; Vafidis et al., 20082). Taxon Orders Oste- Larvae indet.1 ichthyes Crusta- Decapoda-Natantia indet.2, Decapoda-Brachyura indet.2, Euphausiacea indet.1,2, cea Mysida indet.2, Amphipoda indet.2, Copepoda indet.1,2, indet.1 Cni- Hydrozoa indet.2 daria 14.7.2 Predators Alloteuthis media is potentially available to demersal fish of medium and large size. The species is eaten by several fish species (Zuev and Nesis, 1971; Mienis, 1980; Matallanas et al., 1995; Bello, 1997; Capapé, 1977; Velasco et al., 2001; Morte et al., 2001, 2002; Cartes et al., 2004; Bozzano et al., 2005; Carpentieri et al., 2005, 2007; Valls et al., 2011) (Table Cephalopod biology and fisheries in Europe: II. Species Accounts | 175 14.3). It is also identified in a fish-stomach-contents database for UK waters (Cefas2), but Alloteuthis beaks in stomach contents are usually not identified to species level because of the difficulty of distinguishing the beaks of the two species. Velasco et al. (2001) recorded Alloteuthis sp. in the diet of 16 fish species, and it was the most important cephalopod category in the diet of blue whiting (Micromesistius poutassou). Table 14.3. Known predators of Alloteuthis media in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopoda Common octopus (Octopus vul- Quetglas et al. (1998a) garis) Musky octopus (Eledone moschata) Krstulović Šifner and Vrgoč (2009b) Chondrich- Lesser spotted dogfish (Scyliorhinus thyes canicula) Longnose spurdog (Squalus blain- Cefas1 Mienis (1980) ville) Osteichthyes Bull ray (Pteromylaeus bovinus) Capapé (1997) Thornback ray (Raja clavata) Bello (1997), Valls et al. (2011) Bicoloured false moray (Chlopis bi- Carpentieri et al. (2007) color) Blacktailed conger (Gnathophis Carpentieri et al. (2007) mystax) European hake (Merluccius merluc- Cartes et al. (2004), Bozzano et al. cius) (2005), Carpentieri et al. (2005) Geater amberjack (Seriola dumerili) Matallanas et al. (1995) Greater forkbeard (Phycis blen- Morte et al. (2002) noides) Poor cod (Trisopterus minutus Morte et al. (2001) capelanus) Cetacea Striped dolphin (Stenella coeruleo- Würtz and Marrale (1993) alba) 14.8 Other ecological aspects 14.8.1 Parasites Anisakis simplex (a nematode of the Anisakidae family) has been identified in A. media from the Northeast Atlantic, for which, however, it is not considered an important host parasite (Smith, 1984). Gestal et al. (1999) reported the copepod Pennella sp. on the gills of several cephalopod species in the Tyrrhenian Sea, including A. media. 14.9 Fisheries Alloteuthis media is taken as bycatch in bottom trawl and beach-seine fisheries. Studies on bottom trawl discards have shown that the species is totally discarded in the northeastern Mediteranean (Machias et al., 2001), whereas it seems to be discarded only accidentally during the fast sorting operations on deck of fishing vessels in the western 2http://www.cefas.defra.gov.uk/our-science/fisheries-information/fish-stomach-records/predators-of-specified-prey.aspx 176 | ICES Cooperative Research Report No. 325 Mediterranean (Sartor et al., 1998a). In the Gulf of Cádiz, the annual landings of Alloteuthis sp. during the period 1996–2004 oscillated between 55 and 290 t, of which 55% were found to correspond to A. media, according to trawl survey data (I. Sobrino, pers. comm.). In general, separate statistics by species are not provided, and where there is an attempt to identify catches to species, catches of A. media are probably reported as Loligo sp. or Alloteuthis sp. 14.10 Future research, needs, and outlook Clarification of the status of the species (and morphotypes) of the genus Alloteuthis is urgently needed. In addition, as with most cephalopod fishery catches, there is a need to ensure that reporting is at species level. This would also facilitate stock assessment of these species, should it be needed. Given their apparent abundance in continental shelf communities, it is likely that they have an important ecological role, and this also merits further studies. Because of its small size, high growth plasticity, and easily interpretable statolith microstructure, A. media might be an ideal species for laboratory studies to investigate how cephalopod growth and life history respond under different temperature and environmental regimes. Such work, as suggested by Jackson (2004), may also help to establish the extent to which loliginids may serve as useful indicators of ecosystem health and climate change. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Illex coindetii Broadtail shortfin squid | 177 178 | 15 ICES Cooperative Research Report No. 325 Illex coindetii (Vérany, 1839) Patrizia Jereb, Drosos Koutsoubas, Paola Belcari, Graham J. Pierce, Roger Villanueva, A. Louise Allcock, and Evgenia Lefkaditou Common names Faux encornet (France), θράψαλο [thrapsalo] (Greece), Totano (Italy), pota-voadora (Portugal), volador (Spain), broadtail shortfin squid (UK) (Figure 15.1). Synonyms Loligo brongniartii Blainville, 1823, Loligo coindetii Vérany, 1839, Loligo pillae Vérany, 1851, Loligo sagittata: Vérany (1851), Illex illecebrosus coindeti: Pfeffer (1912). 15.1 Geographic distribution The broadtail shortfin squid, Illex coindetii (Vérany, 1839), is found on both sides of the Atlantic and throughout the Mediterranean Sea (Roper et al., 1998) (Figure 15.2). In the Northwest Atlantic, it is found from off the northeast coast of the United States (i.e. 37°N, Roper et al., 1998) south to ca. 3°N (Roper et al., 1998). In the Northeast Atlantic, it has been reported from as far north as Oslo Fjord, Norway (59°N; Lu, 1973) and the Firth Figure 15.1. Illex coindetii. Dorsal view. of Forth, east Scotland (Norman, 1890), down From Guerra (1992). to Namibia, between Hollam’s Bird Island (24°S), and Cape Frio (18°S) (Roeleveld, 1998). It is found in the North Sea, though rarely (e.g. Grimpe, 1925; Oesterwind et al., 2010), but it is not mentioned among the species listed in Swedish waters by Hornbörg (2005). Its extends south and west through the English Channel (Norman, 1890; Marine Biological Association of the United Kingdom, 1931) to the Bristol Channel (Roper et al., 1998), and records exist of it in the Irish Sea (Isle of Man; Moore, 1937, in Stephen, 1944). Although not listed among cephalopod species of the Irish coast by Massy (1928), it is commonly caught by commercial trawl west of Ireland (Lordan et al., 1998b, 2001a), and it is also very common in southwestern Irish waters and in the Celtic Sea (Lordan et al., 2001a). Illex coindetii is widely distributed and abundant along the French and Iberian coasts (see references in Adam, 1952; Guerra et al., 1994; Arvanitidis et al., 2002) and throughout the Mediterranean Sea (Mangold and Boletzky, 1987; Bello 2004; Salman, 2009), including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Soro and Paolini, 1994; Krstulović Šifner et al., 2005; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b; Duysak Cephalopod biology and fisheries in Europe: II. Species Accounts | 179 et al., 2008). It has been recorded in the Sea of Marmara (Katağan et al., 1993). Figure 15.2. Illex coindetii. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 15.2 Taxonomy 15.2.1 Systematics Coleoidea – Decapodiformes – Oegopsida – Ommastrephidae – Illicinae – Illex. 15.2.2 Type locality Off Nice, France, western Mediterranean Sea. 15.2.3 Type repository National Museum of Natural History, Smithsonian Institution, PO Box 37012, MRC 153Washington, DC 20013-7012, USA. Neotype 727457 [fide Roper et al. (1998)]. 15.3 Diagnosis 15.3.1 Paralarvae Ommastrephid squids, including Illex species, produce some of the smallest cephalopod eggs, which yield unique “rhynchoteuthion” hatchlings, less than 2 mm total length (e.g. O’Dor et al., 1985). They have only two pairs of arms and a proboscis, which later divides to form the tentacles in the adults. The proboscis is ca. 50–75% of the length of the mantle. Division of the proboscis begins at ca. 4 mm ML and is completed by 10 mm ML. Common features at this paralarval stage are the absence of ocular or visceral photophores and the presence of nearly equal-sized suckers on the proboscis tip. According to Sweeney et al. (1992), these youngest forms of Illex coindetii, I. argentinus, I. illecebrosus, and I. oxygonius cannot be distinguished from each other. However, 180 | ICES Cooperative Research Report No. 325 research focused on distinguishing features of the early life stages of I. coindetii from the Mediterranean Sea is currently underway using in vitro fertilization techniques (see Villanueva et al., 2011). 15.3.2 Juveniles and adults The morphology of the species is highly variable, mainly because of the marked sexual dimorphism and the resulting divergence in growth pattern of several body dimensions (mantle, head, arms) during maturation (Mangold et al., 1969; Lleonart et al., 1980; Sánchez, 1983; Hernández-García and Castro, 1998; Lefkaditou, 2006; Petrić et al., 2010). As there are several morphotypes throughout the species’ distribution (Roper et al., 1998; Roper and Mangold, 1998), only basic morphological features are reported below. The arms bear two longitudinal series of suckers, and the tentacular club dactylus bears 8 longitudinal series of minute, subequal suckers. The largest sucker rings on the manus of the club are notched, forming low, truncate to blunt, rounded crenulations either in the distal half or all around; they are not smooth (Figure 15.3). The tentacle fixing apparatus is weakly developed. Either the left or the right ventral arm of the male is hectocotylized, with the Figure 15.3. Illex coindetii. Sucker modified portion ranging in length from 15 to rings of arm (left) and tentacle (right). 33% of the arm length. The distal trabeculae are Photo: Evgenia Lefkaditou. modified to form papillary flaps. The length of the suckerless portion at the base of the hectocotylized arm is ca. 13% of the total arm length, and this character is very useful for distinguishing I. coindetii from congeneric species. The head–width index is large: 23 (19–26) in mature males and 19 (15–22) in mature females. Lower beaks have long and strong jaw edges, and upper beaks have long and strong hoods. The funnel cartilage has an inverse T-shape. Fins are short and slightly rhomboid, and their width equates to ca. 45–60% of mantle length (ML). Mantle width is 15–25% of ML. The funnel groove lacks both a foveola and lateral pockets (Roper et al., 1998; Roper and Mangold, 1998). 15.4 Remarks A record of the species at 30°W in the North Atlantic exists (Clarke, 1966, Figure 10[2], p. 120). However, no mention of that finding is reported in Clarke’s text, and no other record of specimens found so far from the continental shelf has been reported subsequently, to the best knowledge of the authors of this review. Presumably, the holotype was deposited in the Museum of Natural History in Nice, but it is neither extant there nor at the Museum National d’Histoire Naturelle, Paris; therefore it is assumed to be lost. Hence, a neotype has been designated: a mature male, 132 mm ML, collected from the Mediterranean Sea (ca. 300 km southwest of Nice), deposited in the National Museum of Natural History, Smithsonian Institution (USNM 727457, Roper et al., 1998). Recent comprehensive analyses seem to indicate that I. coindetii from the Atlantic and Mediterranean belong to a single, widely distributed, highly plastic and variable species (Roper and Mangold, 1998; Martínez et al., 2005a, b; Carlini et al., 2006). However, specimens from different areas sometimes differ strikingly from the “typical” Illex from the Catalonian region (Roper and Mangold, 1998). These morphotypes are neither well Cephalopod biology and fisheries in Europe: II. Species Accounts | 181 defined nor fully understood at present and seem related not only to geographic distribution, but also to local and regional environmental factors; all of these may affect metabolic rates, maturity, growth rates, and morphometric divergence as a consequence of sexual dimorphism (Hernández-García and Castro, 1998). Therefore, a general consensus exists on the need for further studies to investigate this variability. While statolith morphometric analysis based on landmarks may prove a useful taxonomic tool to distinguish I. coindetii from closely related species (Lombarte et al., 2006), hectocotylus, left ventral arm features in females and beak morphometry offer ways to investigate intraspecific variation (Martínez et al., 2002; Petrić et al., 2010). 15.5 Life history The life cycle of I. coindetii is probably annual, even though shorter (6–8 months) and longer (18 months) lifespans have been estimated using different techniques in different areas. Spawning is year-round, with seasonal peaks. 15.5.1 Egg and juvenile development Eggs are small (0.8–1.3 mm) (Boletzky et al., 1973; Hernández-García, 2002a; Villanueva et al., 2011) and are probably laid on the continental slope in midwater. The egg jelly is completely transparent (Boletzky et al., 1973), and the egg chorion swells markedly during embryonic development. Laboratory observations indicate that chorion expansion is strictly dependent on the presence of oviducal jelly, because fertilized eggs not treated with oviducal jelly show no chorion expansion, which results in 100% embryo mortality (Villanueva et al., 2011). Nidamental gland jelly probably also plays an important role in optimal egg development, even though its function is still poorly understood (see Villanueva et al., 2011, for detail). Illex coindetii eggs at hatching are ca. 2 mm long (Boletzky et al., 1973; Villanueva et al., 2011). The success and duration of embryonic development is related to water temperature. All observations available to date indicate that successful embryonic development for I. coindetii takes ca. 10–14 d at 15°C; this temperature corresponds to the median temperature value reported for Mediterranean Sea midwater (Villanueva et al., 2011), where the egg masses are suspected to float. Even though a thorough morphological description is not yet available, embryos of I. coindetii were first observed in the laboratory by Boletzky et al. (1973), and paralarvae have been collected off the Spanish Mediterranean coasts (Sánchez and Moli, 1985) and in the eastern Mediterranean (Salman, 2012) more recently. Embryos and newly hatched squids have been photographed by Villanueva et al. (2011) and are shown in Figure 15.4. Young individuals are described as active swimmers; they use jet propulsion typical of planktonic cephalopod paralarvae, adopting a head-down, oblique position (Boletzky et al., 1973). 182 | ICES Cooperative Research Report No. 325 15.5.2 Growth and lifespan Illex coindetii is a medium-sized squid, commonly reaching 200–250 mm ML throughout its distributional range (Roper et al., 2010a). The maximum mantle lengths recorded for females and males are 379 and 279 mm, respectively (Northeast Atlantic; González et al., 1994b, 1996a). The maximum size of 320 mm ML reported for males in Sánchez et al. (1998b), with no specific reference to the record, is probably erroneous. Females are larger than males, and maximum size varies depending on the population examined (see Table 15.1). Very large specimens of ≥300 mm ML are occasionally captured on both sides of the Atlantic and in the Mediterranean (e.g. GonzáFigure 15.4. Illex coindetii. Eggs and lez et al., 1996a; Roper et al., 1998; Ceriola et hatchlings. Scale = al., 2006; Perdichizzi et al., 2011). However, 0.5 mm. Photos: these represent extremes in the populations Roger Villanueva. and may be late-hatching members of the previous year class or individuals that, for some reason, do not reach maturity, do not spawn, and continue to grow, a phenomenon that has been suggested for other squid species (e.g. Verrill, 1881, in Roper and Mangold, 1998; Cuccu et al., 2005). Table 15.1. Illex coindetii. Maximum mantle length (mm) for females (F) and males (M) in different geographic areas of the Northeast Atlantic and Mediterranean Sea. Region ML (mm) Reference F M Northeast Atlantic 379 279 González et al. (1994b) Portuguese Atlantic 286 217 Arvanitidis et al. (2002) Northwest African coast 300 230 Arkhipkin (1996) Spanish Mediterranean 170 140 Sánchez (1984) French Mediterranean 263 200 Mangold-Wirz (1963a) Northern Tyrrhenian Sea 245 175 Belcari et al. (1989b) Central Tyrrhenian Sea 200 Southern Tyrrhenian Sea 300 210 Perdichizzi et al. (2011) Sicilian Channel 230 180 Jereb and Ragonese (1995) Southwestern Adriatic Sea 220 (300*) 200 Ceriola et al. (2006) Western Adriatic Sea 280 183 Soro and Paolini (1994) Eastern Adriatic Sea 216 187 Petrić et al. (2010) Northern Aegean Sea 240 182 Lefkaditou (2006) Levantine Basin (Cyprus) 180 145 Salman et al. (1998) Gentiloni et al. (2001) * Only one specimen, not considered in calculations. Based on length frequency analyses, the maximum lifespan of I. coindetii from different Cephalopod biology and fisheries in Europe: II. Species Accounts | 183 geographic areas has been estimated to be 12–18 months, whereas direct age determination by statolith reading has indicated lifespans as short as 6 months (Table 15.2). Length frequency distributions for cephalopod species of interest to fisheries are generally polymodal, but it is difficult to identify microcohorts, and growth estimates by means of length frequency methods are difficult to make (Sánchez, 1984; Caddy, 1991; Jereb and Ragonese, 1995; Arvanitidis et al., 2002). Therefore, direct age determination methods are applied more frequently. Despite the acknowledged validity of the methodology (Jereb et al., 1991; Jackson, 1994; Ceriola and Milone, 2007), several authors have advised caution in interpreting age values from statolith readings (e.g. Lipiński and Durholtz, 1994; González et al., 2000; Bettencourt and Guerra, 2001). Growth rate (see Table 15.2) is high, faster in females than in males, and often two or more groups are identifiable in the population, each with different growth rhythms, depending on the hatching period (Jereb and Ragonese, 1995; Sánchez, 1995; Belcari, 1996; González et al., 1996a; Arkhipkin et al., 2000; Ragonese et al., 2002). Spring–summer hatched squids grow faster than autumn–winter hatchings. González et al. (1996a) measured instantaneous relative growth rate as well as absolute growth rate. Although there was considerable variation, the fastest relative growth rate was recorded in 6month-old individuals of both sexes (1.33% ML d –1 and 4.49% BW d–1 in males; 1.73% ML d–1 and 5.06% BW d–1 in females) and the slowest growth in 13-month-old males (0.10% ML d–1 and 0.03% BW d–1) and 14-month-old females (0.18% ML d–1 and 0.81% BW d–1). Table 15.2. Illex coindetii. Growth rates (absolute values) and lifespan of populations from the Northeast Atlantic and Mediterranean Sea. Metho Growth rate (mm d– d 1) DA DA Lifespan (months) F M F M 1.11 - 12 12 0.72 0.84 13 15 Region Reference Northeast At- Sánchez et al. lantic (1998b) Galician wa- González et al. ters (1996a) DA - - 8 6 Sierra Leone Arkhipkin (1996) DA - - 10 8 West Sahara Arkhipkin (1996) DA 0.44 - 18 18 Western Medi- Sánchez et al. terranean (1998b) Sicilian Chan- Arkhipkin et al. nel (2000) DA DA 1.55 1.78 6–7 0.06– 0.06– 1.17 1.09 0.39– 0.33– 0.43 0.34 CM 0.47 0.38 17.7 MPA 0.67 0.73 18 CM 13.5 24 6–7 14.5 Northern Ae- Lefkaditou et al. gean (2007) Western Medi- Mangold-Wirz terranean (1963a) 16.6 Catalan Sea Sánchez (1984) 11 Southern Arvanitidis et al. Celtic (2002) 12–20 Sea – Bay of Biscay MPA 0.50– 0.30– 0.86 0.83 15 15 Galician waters González (1994) 184 | ICES Cooperative Research Report No. 325 MPA 0.92 MPA MPA - 0.32– 0.32– 0.45 0.45 0.82 0.84 13 14–16 15 - 14–16 10 Portuguese Arvanitidis et al. waters (2002) Sicilian Chan- Jereb and Rago- nel nese (1995) Greek Seas Arvanitidis et al. (2002) DA = direct ageing using statoliths; CM = cohort monitoring, MPA = modal progression analysis. F=female. M=male. Sexual differences in the length–weight relationship exist (Table 15.3). Values of the coefficient b are always lower in females, reflecting morphometric sexual dimorphism of adult animals, whereby males exhibit a marked increase in head and arm robustness and become heavier than females at same length (e.g. Belcari, 1996; Ceriola et al., 2006). Table 15.3. Illex coindetii. Length–weight relationships in different geographic areas for females (F) and males (M). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Southern Celtic 0.058 2.76 F Arvanitidis et al. (2002) 0.296 3.17 M 0.033 2.91 F 0.022 3.16 M 0.016–0.017 3.09–3.12 F 0.006–0.007 3.57–3.58 M 0.046 2.76 F 0.016 3.30 M 0.027–0.041 2.89–3 F 0.017–0.040 3.02–3.24 M 0.022 3.04 F 0.011 3.39 M 0.043–0.046 2.79–2.83 F Sea – Bay of Biscay Northwestern Spanish González et al. (1996a) waters Portuguese waters Catalan Sea Northern Tyrrhenian Sea Sicilian Channel Sánchez et al. (1998b) Arvanitidis et al. (2002) Sánchez et al. (1998b) Belcari (1996) Ragonese and Jereb (1992) 0.021–0.022 3.19–3.21 M 0.002 3.02 F 0.016 3.45 M 0.030 3.00 F 0.011 3.58 M 0.047 2.83 F 0.018 3.25 M Iskenderun Bay 0.019 3.16 F (northeastern Levant 0.018 3.29 M Central eastern Adriatic Petrić et al. (2010) Sea Southwestern Adriatic Ceriola et al. (2006) Sea Greek Seas Arvanitidis et al. (2002) Duysak et al. (2008) Sea) 15.5.3 Maturation and reproduction Sex ratios close to 1:1 have been recorded in most of the populations studied (e.g. Jereb Cephalopod biology and fisheries in Europe: II. Species Accounts | 185 and Ragonese, 1995; Sánchez et al., 1998b; Arvanitidis et al., 2002; Ceriola et al., 2006); significant deviations have been recorded only in Galician waters (González and Guerra, 1996) and in the Ionian Sea (Tursi and D’Onghia, 1992). Age at maturation varies between 120 and 271 d in males and between 120 and 285 d in females, depending on the geographic area and season considered (González et al., 1996a; Arkhipkin et al., 1998). Individuals of this species mature at a wide range of sizes. Although size at maturity shows some degree of geographic variation in both sexes (e.g. Arvanitidis et al., 2002; Hernández-García, 2002a), males mature at a lower minimum size than females. Also, a west–east gradient of decreasing mantle length values at maturity has been found in populations from the Atlantic to the eastern Mediterranean (Table 15.4). Table 15.4. Illex coindetii. Size at 50% maturity (MLm50%) in populations from different geographical areas of the eastern Atlantic and Mediterranean Sea. Region MLm50% (mm) Reference Females Males Southern Celtic Sea – Bay of Biscay 248 153 Arvanitidis et al. (2002) Galician waters 184 128 González and Guerra (1996) Portuguese waters 191 129 Arvanitidis et al. (2002) Eastern Atlantic 172–218 127–166 Hernández-García (2002a) Western Mediterranean 150 120 Sánchez et al. (1998b) Central Tyrrhenian Sea 120 105 Gentiloni et al. (2001) Southern Tyrrhenian Sea 150 105 Perdichizzi et al. (2011) Sicilian Channel 150 120 Jereb and Ragonese (1995) Adriatic Sea 146 137 Ceriola et al. (2006) Eastern Ionian Sea 140–187 120–152 Lefkaditou et al. (2008) Aegean Sea 146–181 113–138 Lefkaditou et al. (2007) Illex coindetii females spawn several times during the spawning period, which may last for several weeks (González and Guerra, 1996). Spawning is year-round, but seasonal peaks exist and vary with area throughout the Mediterranean and Atlantic (e.g. González and Guerra, 1996; Sánchez et al., 1998b; Belcari, 1999c; Ceriola et al., 2006; Lefkaditou et al., 2007). This variability is thought to be related to differences in water temperature (Arvanitidis et al., 2002; Hernández-García, 2002a). Reproductive outputs in males and females vary with body size. Approximately 800 000 oocytes were recorded in a 250 mm ML female (Laptikhovsky and Nigmatullin, 1993), and 1555 spermatophores were counted in a mature male of 245 mm ML (González and Guerra, 1996). Spermatophore length varied between 14 and 38 mm. 15.6 Biological distribution 15.6.1 Habitat Illex coindetii has been recorded from surface waters to >1000 m, but concentrations peak between 100 and 400–600 m, depending on the geographic area considered (Roper et al., 2010a). It lives close to muddy, sandy, and debris-rich bottoms, which are often covered by Funiculina spp. in the middle and lower sublittoral and upper bathyal domains (Roper et al., 2010a). It has been found associated with decapod crustaceans, such as the deep-water rose shrimp (Parapenaeus longirostris), and, more significantly, with 186 | ICES Cooperative Research Report No. 325 fish such as the European hake (Merluccius merluccius) and the blue whiting (Micromesistius poutassou) (Jereb and Ragonese, 1991b; Rasero et al., 1996; Dawe and Brodziak, 1998), often along with the lesser flying squid (Todaropsis eblanae) (MangoldWirz, 1963a; Lumare, 1970; Rasero et al., 1996; Dawe and Brodziak, 1998; Ciavaglia and Manfredi, 2009; Silva et al., 2011), but also with the horned octopus (Eledone cirrhosa) and the midsize squid (Alloteuthis media) (Krstulović Šifner et al., 2005, 2011; Silva et al., 2011). Juveniles and adults share the same depth range in some areas of the Mediterranean (Sánchez et al., 1998b; Ceriola et al., 2006), even though a major concentration of small specimens is observed in shallower waters (<200 m). Large and mature squids were found throughout the whole depth range (Sánchez et al., 1998b). The presence of upwelling of cold waters rich in nutrients and contributing to high productivity in the area near Gibraltar is considered to influence positively the presence and abundance of I. coindetii on the slope and upper shelf of the Gulf of Cádiz (Silva et al., 2011). However, mature animals, especially females, have been reported to concentrate in regions with lower upwelling activity in Greek waters (Lefkaditou et al., 2008); it has been suggested that concentrations in relatively more protected areas may be related to “spatial protection” of paralarvae, assuming that hatching areas are close to the spawning areas. 15.6.2 Migrations Adults, at least, undergo vertical migrations from the bottom to the upper layers at night, even though they remain below the thermocline (Sánchez et al., 1998b). Seasonal migrations have been observed in the French Mediterranean and the Catalan Sea (Mangold-Wirz, 1963a; Sánchez et al., 1998b), with the bulk of the population seeking shallow waters (70–150 m) in spring, where they remain all summer. In autumn and winter, the population spreads over a wide bathymetric range. 15.7 Trophic ecology 15.7.1 Prey Like most muscular, fast-swimming ommastrephids, I. coindetii is an opportunistic predator (e.g. Rasero et al., 1996; Sánchez et al., 1998b; Lordan et al., 1998b; Lelli et al., 2005). The diet is composed of fish, crustaceans, and cephalopods, in decreasing order of importance (Sánchez, 1982; Rasero et al., 1996; Lordan et al., 1998b; Sánchez et al., 1998b; Lelli et al., 2005) (Table 15.5). Usually, one of these main groups is dominant, depending on prey availability and size of squid. Food composition changes with growth (Lordan et al., 1998b) and are related to important changes in squid mouth structures (Castro and Hernández-García, 1995), foraging behaviour, and prey availability in the water column, as well as to increasing body size. As the squid grow, fish and squid become increasingly important prey, and cannibalism may occur, although it is probably of minor importance, except in conditions of very high squid abundance or scarcity of other prey (Dawe and Brodziak, 1998). There are no significant differences in the diets of males and females, although significantly more mature females than mature males have prey remains in their stomachs (Rasero et al., 1996; Lordan et al., 1998b), which has been interpreted as implying that the increasing energetic demands of gonad development is fulfilled by feeding (Rosa et al., 2005b). Cephalopod biology and fisheries in Europe: II. Species Accounts | 187 Throughout its life cycle, I. coindetii is likely to compete actively for prey with other cephalopods and fish. However, although all cephalopod hatchlings begin to feed immediately as predators (Boletzky and Hanlon, 1983), attempts to feed rhynchoteuthions have not been successful (Balch et al., 1985). A peculiar “suspension feeding mechanism” has been suggested for these early life stages (O’Dor et al., 1985). Table 15.5. List of the main identified prey from Illex coindetii stomach contents (compiled from Hernández-García, 19921, Castro and Hernández García, 19952, Rasero et al., 19963, Lordan et al., 1998b4, Sánchez et al., 1998b 5, Stowasser, 20046, Lelli et al., 20057; Lefkaditou 20068; Vafidis et al., 20089; Petrić et al., 201110). Taxon Species Osteichthyes Acropomatidae Synagrops microlepis (thinlip splitfish)1,5 Ammodytidae Gymnammodytes semisquamatus (smooth sandeel)3, indet.6 Argentinidae Argentina sphyraena (argentine)3,4, Argentina spp.4, Glossanodon leioglossus (small-toothed argentine)4 Carangidae Trachurus trachurus (Atlantic horse mackerel)3,4,10 Cepolidae Cepola macrophthalma (red bandfish)3 Centracanthi- indet.7 dae Chlorophthalmi- Chlorophthalmus atlanticus (Atlantic greeneye)5 dae Clupeidae Sardina pilchardus (European pilchard)5,7, Alosa alosa (allis shad)7, Sprattus sprattus (European sprat)3, indet.7 Congridae indet.6 Engraulidae Engraulis encrasicolus (European anchovy)5,7 Epigonidae Epigonus telescopus (black cardinal fish) 2,5 Gadidae Gadiculus argenteus (silvery pout)3,4,5,7,8,10, Micromesistius poutassou (blue whiting)3,4,5,7, Phycis blennoides (greater forkbeard)10, Trisopterus minutus (poor cod)10, indet.6,7 Gobiidae Aphia minuta (transparent goby)3,4, Gobiusculus flavescens (twospotted goby)3, indet.3,4,6,7 Lotidae Gaidropsarus biscayensis (Mediterranean bigeye rockling)5, G. macrophthalmus (big-eyed rockling)3, G. vulgaris (three-bearded rockling)3, Gaidropsarus spp.8, indet. larvae4 Macrouridae indet.7 Merlucciidae Merluccius merluccius (European hake)3,4,7 Myctophidae Ceratoscopelus maderensis (Madeira lanternfish)5,8, Diaphus dumerelii1,2, Diaphus spp.1,4,8, Hygophum benoiti(Benoit's lanternfish)8, Lampanyctus crocodilus (jewel lanternfish)5, Myctophum punctatum (spotted lanternfish)5, Notoscopelus elongatus (elongated lanternfish)5,8, indet.7 Paralepididae Sudis hyalina (baracundina)5 Pleuronecti- indet.3 formes Scombridae Scomber colias (Atlantic chub mackerel)5, Scomber scombrus (Atlantic mackerel)4 Scorpaenidae indet.7 Soleidae Microchirus boscanion (Lusitanian sole)2, Solea spp.2 188 | ICES Cooperative Research Report No. 325 Sparidae Dentex spp.2, Diplodus spp.2,3 Sternoptychidae Argyropelecus hemigymnus (half-naked hatchetfish)4, Maurolicus muelleri (pearlside)2,3,4,5,7,8,10 Triglidae indet.7 Zeidae Zeus faber (John dory)3 Crustacea Decapoda Dendrobranchi- indet.6 Parapenaeus longirostris5, Penaeidae indet.1 ata-Penaeiodea Macrura reptan- indet.7 tia Pleocyemata- Polybius henslowii3, indet.7 Brachyura Pleocyemata- Alpheus glaber5, Crangonidae indet.7, Dichelopandalus bonnieri4, Caridea Pandalidae indet.2, Pasiphaea sivado1,2,5, 7, P. multidentata5, Pasiphaea spp.3,4,5,7, Plesionika heterocarpus1,5, Plesionika martia3, Plesionika spp.2,5,7, Sergia robusta (as Sergestes robustus)3, Sergestidae indet.7 Stomatopoda indet.6 Euphausiacea Euphasia spp.5, Meganyctiphanes norvegica3,4,5, Nyctiphanes couchii5, Thysanopoda spp.2, indet.4,6,9 Mysida indet.5,6,7,9 Amphipoda Gammaridea indet.3, Vibilia armata5, indet.2,5,7,9 Copepoda Oncaea spp.5, Calanoida indet.7, indet.5,6 Cephalopoda Myopsida Alloteuthis subulata3, Alloteuthis spp.2,4, Loligo forbesii4, Loligo spp.2,3,5, Loliginidae indet.6 Oegopsida Abralia veranyi2, Enoploteuthidae indet.1, Histioteuthidae indet.7, Illex coindetii2,3,4,5,7,10, Ommastrephidae indet.1,6,7, Onychoteuthidae indet.1, Onychoteuthis banksii7, Todarodes sagittatus4, Todaropsis eblanae2,3,4,5,7,10 Octopoda Sepioidea Octopus spp.2, indet.7 Rossia macrosoma4,7, Sepia bertheloti2, S. orbignyana1, Sepia spp.1,2, Sepietta oweniana4,7, Sepiolidae indet.4,5,6,7, indet.7 Gastropoda Heliconoides inflatus7, Limacina retroversa (retrovert pteropod)4, indet.7 Bivalvia indet.7 Tunicata indet.5,9 Chaetognatha indet.5 15.7.2 Predators No information on predators of larval and small juveniles of Illex is available at present (Dawe and Brodziak, 1998). Adults are found in the stomachs of various cetaceans, bony fish, and sharks, as well as being eaten by other squid species (Table 15.6). Cephalopod biology and fisheries in Europe: II. Species Accounts | 189 Table 15.6. Known predators of Illex coindetii in the Northeast Atlantic and Mediterranean Sea. Taxon Species References Cephalopoda European squid (Loligo vulgaris) Dawe and Brodziak (1998) European flying squid (Todarodes Dawe and Brodziak (1998) sagittatus) Chondrich- Black-mouthed dogfish (Galeus thyes melastomus) Lesser spotted dogfish (Scyliorhi- Valls et al. (2011) Kabasakal (2002) nus canicula) Sharpnose sevengill shark (Hep- Henderson and Williams (2001) tranchias perlo) Shortfin mako (Isurus oxyrinchus) Maia et al. (2006) Smooth-hound (Mustelus mus- Kabasakal (2002) telus) Thornback ray (Raja clavata) Kabasakal (2002), Farias et al. (2006), Šantić et al. (2012) Osteichthyes Albacore (Thunnus alalunga) Consoli et al. (2008), Romeo et al. (2012) Atlantic bluefin tuna (Thunnus Karakulak et al. (2009), Romeo et al. thynnus) (2012), Battaglia et al. (2013) Blonde ray (Raja brachyura) Farias et al. (2006) Blue whiting (Micromesistius Macpherson (1978) poutassou) Common dolphinfish (Cory- Massutí et al. (1998) phaena hippurus) Conger eel (Conger conger) Lordan et al. (1998b) Greater forkbeard (Phycis blen- Morte et al. (2002) noides) Mediterranean spearfish (Tetrap- Castriota et al. (2008), Romeo et al. turus belone) (2009, 2012) Saithe (Pollachius virens) Lordan et al. (1998b) Smooth lanternshark (Etmopterus Xavier et al. (2012) pusillus) Swordfish (Xiphias gladius) Bello (1985), Moreira (1990), Salman (2004), Peristeraki et al. (2005), Romeo et al. (2009, 2012) Yellowfin tuna (Thunnus alba- Dragovich (1970) cares) Cetacea Bottlenose dolphin (Tursiops trun- González et al. (1994a), Santos et al. catus) (1997) Common dolphin (Delphinus del- González et al. (1994a), Silva (1999a) phis) Long-finned pilot whale (Globio- González et al. (1994a) cephala melas) Risso’s dolphin (Grampus griseus) Carlini et al. (1992), González et al. (1994a), Santos et al. (1997), Blanco et al. (2006), Bearzi et al. (2011) Striped dolphin (Stenella coerule- Würtz and Marrale (1993), Alessandri oalba) et al. (2001) 190 | 15.8 ICES Cooperative Research Report No. 325 Other ecological aspects 15.8.1 Parasites Illex coindetii is one of the most important cephalopod paratenic hosts in the life cycle of several parasites, such as cestodes of the genus Phyllobothrium and nematodes such as Anisakis simplex and A. physeteris (Pascual et al., 1994, 1995, 1996a, 1999; Abollo et al., 1998; Gestal et al., 1999; Petrić et al., 2011); it also appears to be infested by copepods of the genus Pennella, especially in some areas of its distribution (Pascual et al., 2001). It functions as a trophic bridge for parasite flow within the marine ecosystem, because it is the prey of the parasites' final hosts (e.g. cetaceans such as Delphinus delphis, Tursiops truncatus, Stenella coeruleoalba, and others). Recent studies have demonstrated for the first time its role as a second, rather than first, paratenic host (Petrić et al., 2011). Additional information on parasites of I. coindetii and T. eblanae (Pascual et al., 1996b) suggests that these species are sympatric and share similar econiches and that parasites may also be useful as an indirect indicator of the migratory habits of the squid. 15.8.2 Environmental effects Recent observations show high correlations between the I. coindetii life cycle and environmental parameters, such as water temperature, trophic enrichments, current regimes, and other oceanographic features (Jereb et al., 2001; Arvanitidis et al., 2002; Ceriola et al., 2006, 2007; Lefkaditou et al., 2008). These results suggest high levels of environmentally driven flexibility for the species. Based on all information gathered, it is likely that I. coindetii, an ommastrephid squid exploited almost exclusively by bottom trawl, can be singled out as a key/indicator species in the context of dynamic environments and high fishing pressure areas, such as some Mediterranean regions (Ceriola et al., 2007). Because of its short life cycle and highly variable abundance levels, it may indicate changes in environmental conditions and fishing pressure, although it may be difficult to disentangle fishing pressure and global warming effects. Recruitment in particular is likely to be affected by environmental conditions (Jereb et al., 2001; Ceriola et al., 2007; Lefkaditou et al., 2008; Cuccu et al., 2009b), because of eggmass properties. Egg masses have never been recorded in nature for Illex species. However, observations in captivity (Durward et al., 1980; O’Dor et al., 1985) showed that Illex species can produce gelatinous egg masses while swimming in open water. Other observations indicate that the gel functions as a buoyancy mechanism that prevents eggs from sinking, and that complete density equilibration requires many days under most conditions (O’Dor et al., 1985). Such a mechanism would retain pelagically spawned eggs of Illex in zones where temperatures are most favourable for embryonic development. In addition, favourable environmental conditions are likely to have a positive effect on the survival of hatchlings and early juveniles. Despite consistency in the location of spawning areas, interannual variability has been observed in the location of main recruitment areas, which could be related to mechanisms such as association with mesoscale eddies, affecting post-hatching dispersal (e.g. Lefkaditou et al., 2008). An increase in the density of recruits in the populations of the southern Adriatic and the eastern Ionian Sea in the mid-2000s may have resulted from a combination of increased temperature in the entire water column of the central Mediterranean, the decline of many I. coindetii predators, and the increased presence of some potential prey in the area investigated (Ceriola et al., 2007; Lefkaditou et al., 2008). Distribution, recruitment, and abundance are closely related to ocean climate variability for the most broadly distributed and most highly migratory congener, Illex illecebrosus (Dawe and Brodziak, 1998). Although such relationships may not hold as strongly for the less migratory I coindetii, only additional time-series of reliable data could help clarify these Cephalopod biology and fisheries in Europe: II. Species Accounts | 191 issues. 15.9 Fisheries Illex coindetii is taken throughout the year in the Mediterranean, off West Africa, and in the Northeast Atlantic as bycatch in bottom and pelagic trawls, and, to a lesser extent, with gill- and trammelnets, in depths of 100–400 m (Mangold and Boletzky, 1987; Jereb and Ragonese, 1995; González et al., 1994b, 1996b; Ceriola et al., 2008; Hastie et al., 2009a; Tosunoğlu et al, 2009). It is of increasing fisheries value and represents a valuable resource in some areas of its distribution range because of the size of the catches (Jereb and Ragonese, 1995). The high interannual variation in ommastrephid landings throughout the Mediterranean and the eastern Atlantic is one of the characteristics of ommastrephid fisheries (Stergiou, 1989; González et al., 1996b; Sánchez et al., 1998b). Also, there is marked seasonality in trawl landings, which varies depending on the area: peaks may arise in summer (e.g. northern Tyrrhenian Sea; Belcari et al., 1998) or winter and spring (e.g. southern Celtic Sea and Bay of Biscay; Arvanitidis et al., 2002). An increasing trend in abundance has been observed in the Ionian Sea in recent decades (Lefkaditou et al., 2008; Maiorano et al., 2010). However, a significant inverse correlation with fishing effort has also been shown (Maiorano et al., 2010), and gear selectivity studies confirm that current legal minimum mesh size and codend configurations for demersal trawling do not favour sustainable fishing for this or other cephalopod species (Tosunoğlu et al., 2009). FAO fishery data (FAO, 2011) for the Mediterranean for the decade beginning in 2000 indicate that landings of I. coindetii have varied from 1800 t in 2003 to >5150 t in 2005; no clear trend is evident. This represents between 3.9 and 7.7% annually of Mediterranean landings of cephalopods. However, it is not clear that the identification to species is reliable. The different ommastrephid species are separated in Spanish landings from ICES Subdivisions VIIIcW and IXaN, based on market sampling. Illex coindetii typically made up ca. 60–80% of monthly ommastrephid landings during the years 1998–2003, the rest being mainly Todaropsis eblanae, although considerable month-to-month fluctuation was evident in both areas, and the proportion was typically much lower (as low as 0%) during several months within the period October–March (Bruno et al., 2009). Although the broadtail shortfin squid is recognized as a separate category in fishery landings by FAO, it is not routinely distinguished from other ommastrephids in most parts of the Northeast Atlantic. During the decade since 2000, up to 450 t of this species have been recorded for the Northeast Atlantic, a small fraction of the 6000–16 000 t of “Various squids nei” landed, a proportion of which could have been I. coindetii. In ICES data, catches of this species are subsumed under the shortfin squid category. Since 2000, annual landings of this category in the European ICES area varied from ca. 5 500 t to as low as 970 t in 2007; the overall trend seems to have been downwards (ICES, 2012). The high interannual variation in ommastrephid landings in the Mediterranean and Northeast Atlantic is typical of ommastrephid fisheries (Stergiou, 1989; González et al., 1996b; Sánchez et al., 1998b). A marked seasonality in trawl landings is also evident, but it varies depending on the area; peaks in summer in the northern Tyrrhenian Sea (Belcari et al., 1998) contrast with peaks in winter and spring in the southern Celtic Sea and Bay of Biscay (Arvanitidis et al., 2002). 192 | ICES Cooperative Research Report No. 325 The analysis of seven populations of I. coindetii from the eastern Atlantic and eastern Mediterranean showed no significant overall genetic differences among samples (Martínez et al., 2005b). Additional comparisons of individuals from the northern Tyrrhenian Sea (western Mediterranean) and Atlantic Iberian waters revealed the presence of a homogeneous population structure, the summer Italian and the spring Atlantic samples being the most divergent (Martínez et al., 2005a). 15.10 Future research, needs, and outlook Like other ommastrephids, I. coindetii plays an essential role in the oceanic system, acting as an ”ecosystem accelerator”. As animals with high food intake and fast conversion rates, these squids function as energy transformers and accumulate high quality proteins, making them available to higher consumers. In addition, the species has a significant commercial value, one that has increased over the past decade, in many parts of Europe. The existence of different morphotypes, neither well-defined nor fully understood at present, related not only to geographic distribution, but also to local and regional environmental factors, should be investigated further. Even though I. coindetii has been a target for research in the past few decades, and rather extensive literature provides sufficient basic information, further detailed studies are required to elucidate its important role as a potential recorder of environmental and ecological change as well as an indicator of possible overexploitation. This will help towards sustainable management of the resource throughout European seas. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Todarodes sagittatus European flying squid | 193 194 | 16 ICES Cooperative Research Report No. 325 Todarodes sagittatus (Lamarck, 1798) Uwe Piatkowski, Karsten Zumholz, Evgenia Lefkaditou, Daniel Oesterwind, Patrizia Jereb, Graham J. Pierce, and A. Louise Allcock Common names Toutenon commun (France), Θράψαλο [thrapsalo] (Greece), totano viola (Italy), pota europeia (Portugal), pota europea3 (Spain), European flying squid (UK) (Figure 16.1). Synonyms Loligo sagittata Lamarck, 1798, Ommastrephes sagittatus (Lamarck, 1798), Loligo todarus Rafinesque, 1814, Sthenoteuthis todarus (Rafinesque, 1814), Ommastrephes todarus (Rafinesque, 1814), Loligo aequipoda Rüppell, 1844, Sepia minor Seba, 1758, Loligo brasiliensis Férussac, 1823, Sepia loligo Gmelin, 1789. 16.1 Geographic distribution The European flying squid (Todarodes sagittatus Lamarck, 1798) has been identified in the North Atlantic from the northeast coasts of Europe to ca. 62°W (Figure 16.2), where it is found associated with the Mid-Atlantic Ridge (Korzun et al., 1979; Vecchione et al., 2010), and from the Arctic Ocean south to the waters off Guinea (Clarke, 1966; Nigmatullin et al., 1998), including northeastern Norway and the Barents Sea (Grieg, 1933; Sennikov and Bliznichenko, 1985), Iceland (Nielsen, 1930; Jonsson, 1998; Figure 16.3), and throughout NorFigure 16.1. Todarodes sagittatus. wegian waters (Nordgård, 1923; Grieg, 1933; WiDorsal view. From Guerra (1992). borg and Beck, 1984). Old records from the Skagerrak (Grimpe, 1925; Jaeckel, 1958) are confirmed by recent information (Hornbörg, 2005), but occasional incursions into the southwestern Baltic Sea (old record in Grimpe, 1925) are rare. Todarodes sagittatus has been recorded in the North Sea, although it is probably limited to the northern area (Oesterwind et al., 2010), and extends past northern Scotland to Shetland waters (Stephen, 1944; Joy, 1990) and south to the west Irish coast (Massy, 1928; Wiborg and Beck, 1984; Lordan et al., 2001a, b), where it is particularly abundant in deep water off the northwest coast (Lordan et al., 2001b). Recorded in the Celtic Sea (Lordan et al., 2001a, b), it extends south through French and Spanish waters, including those of the Azores and Madeira (Magaz, 1934; Bouxin and Legendre, 1936; Rees and Maul, 1956; Piatkowski et al., 1998). Its southernmost records are at 11°N off Guinea (V. Laptikhovsky, pers. comm.). Todarodes sagittatus is widely distributed in the Mediterranean (Mangold and 3 Other common names are also used, e.g. calamar volador (i.e. flying squid). Cephalopod biology and fisheries in Europe: II. Species Accounts | 195 Boletzky, 1987; Bello, 2004; Salman, 2009), including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Bello, 1985; Casali et al., 1988; Krstulović Šifner et al., 2005), the Ionian Sea (Tursi and D’Onghia 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin (D’Onghia et al., 1992; Salman et al., 1997, 1998; Lefkaditou et al., 2003b). Reference to its presence in the Sea of Marmara exists (Demir, 1952, in Ünsal et al., 1999), but it was not recorded during more recent research carried out in those waters (Katağan et al., 1993; Ünsal et al., 1999). Figure 16.2. Todarodes sagittatus. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 16.2 Taxonomy 16.2.1 Systematics Coleoidea – Decapodiformes – Oegopsida – Ommastrephidae – Todarodinae – Todarodes. 16.2.2 Type locality Atlantic Ocean: “sur les côtes de l’Ocean de l’Europe et de l’Amerique”, fide Lamarck (1799: 14). 16.2.3 Figure 16.3. Todarodes sagittatus. Stamps document its distribution in the Northeast Atlantic. Type repository Originally Muséum National d'Histoire Naturelle, Laboratoire Biologie Invertebres Marins et Malacologie, 55, rue de Buffon, 75005 Paris 05, France. MNHN Synypes; specimens not extant [fide Lu et al. (1995)]. 196 | 16.3 ICES Cooperative Research Report No. 325 Diagnosis 16.3.1 Paralarvae Early life stages of T. sagittatus (Figure 16.4) are not well known. Key characters that would allow the distinction of early stages and particularly its paralarvae from those of the other common ommastrephid species in European waters, Illex coindetii and Todaropsis eblanae, have not yet been established (Sweeney et al., 1992; Villanueva et al., 2011). Although the paralarvae of T. sagitattus have not been described, records exist from various regions of the Northeast Atlantic as well as speculations about the location of spawning grounds (e.g. Shimko, 1989; Collins et al., 2002). Figure 16.4. Todarodes sagittatus. Early life stage, 18 mm total length, sampled off Messina, Sicily. Photo: Alberto Villari. 16.3.2 Juveniles and adults This squid is one of the typical muscular cephalopods inhabiting open waters of the high seas (Clarke, 1966; Zuev et al., 1976). Figure 16.5. Todarodes sagittatus. Sucker rings of arm (left) and tentacle (right). Photo: Evgenia Lefkaditou. The fins are wide and strong, with fin length up to 45% of mantle length. The funnel groove has a foveola without side pockets. The suckers on the dactylus of the tentacular club are arranged in four series. The carpus is elongated with 10–12 pairs of suckers. The entire club is relatively long, extending along the stalk. The arm sucker rings have an enlarged central tooth, 7–9 regular teeth, and virtually no small alternating teeth (Figure 16.5). There are no light organs on the viscera. Right arm IV is hectocotylized in males by the modification of terminal suckers into fleshy papillae (Roper et al., 1984; Warneke-Cremer Figure 16.6. Todarodes sagittatus. Lower beak (left) and upper beak and Dzwillo, 1993; (right). Photo: Karsten Zumholz. Roper et al., 2010a). Sexual dimorphism in T. sagittatus results in relatively longer arms and tentacular clubs in females than in Cephalopod biology and fisheries in Europe: II. Species Accounts | 197 males, contrary to the situation in the other two common ommastrephids of European waters, I. coindetii and T. eblanae (Mangold-Wirz, 1963b). The appearance and growth of the mandibles (beaks, Figure 16.6) are described by Hernández-García et al. (1998b). 16.4 Life history Most individuals probably live 12–14 months, but the lifespan of the largest individuals may approach 2 years. Spawning is seasonal, its timing varying with geographic location. 16.4.1 Egg and juvenile development There is no information available on egg and juvenile development. 16.4.2 Growth and lifespan A maximum mantle length of 75 cm was reported for an unsexed specimen from North Atlantic waters (probably a female; Herzenstein, 1885), whereas the maximum recorded mantle length for a male in this area is currently 64 cm (Fridriksson, 1943). In the Mediterranean, the maximum sizes recorded are 60 cm (females) and 38.5 cm (males) (Cuccu et al. 2005). In the North Sea, maximum reported mantle length is 49 cm, and females are larger than males in winter (Oesterwind, 2011), as also reported for several different areas (ICES Divisions IV, V, VI) of the Northeast Atlantic by Lordan et al. (2001b). Common sizes range in general between 35 and 40 cm and 20 and 25 cm for females and males, respectively. The periodicity of statolith increment formation has not been yet validated for the species, although daily growth rings have been confirmed for the congeneric Todarodes pacificus (Nakamura and Sakurai, 1991), as well as for several other ommastrephids, and might, therefore, be assumed for this species. However, assuming that growth increments in statoliths are daily, Rosenberg et al. (1981) estimated a mean absolute growth rate of 2 mm d–1 for individuals with a dorsal mantle length range of 15–52 cm. Moustahfid (2002) estimated that growth rates in squid aged 4–6 months ranged from 0.4 mm d–1 to 1.3 mm d–1 and 0.3 g d–1 to 2.7 g d–1. Instantaneous relative growth rates (G) were 0.6% for ML and 3.4% for BW. Borges and Wallace (1993) estimated growth rates in Norwegian waters from monthly length frequency distributions. Results varied between years, being 0.8–1.2 mm d–1 in females and 0.6–1.0 mm d–1 in males. Instantaneous growth rates (in terms of weight) were estimated as 1.1–1.6% BW d–1 for animals in the weight range 252–322 g. Length–weight relationships have been documented for several geographic areas (Table 16.1). Table 16.1. Todarodes sagittatus. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a B Sex Reference North Sea 0.0078 3.29 F Oesterwind (2011) 0.0075 3.27 M 0.0091 3.23 F Off Norway Borges and Wallace (1993) Off Scotland 0.0111 3.17 M 0.0071 3.33 F 198 | ICES Cooperative Research Report No. 325 Southwestern Portugal, Madeira Northwest African waters Western Mediterranean Eastern Mediterranean 0.0061 3.39 M 0.0158 3.12 F 0.0164 3.09 M 0.0423 2.803 All Arkhipkin et al. (1999) 0.0326 2.991 F Nigmatullin et al. (2002) 0.0314 2.845 M 0.009 3.334 F 0.011 3.282 M 0.0193 3.11 F 0.0081 3.39 M Piatkowski et al. (1998) Quetglas et al. (1998b) E. Lefkaditou, pers. comm. Prior to statolith studies, individuals >50 cm were believed to be at least 2 years old (Nesis, 1982/1987), but most recent studies based on statolith increments have suggested a longevity of not more than 14 months for individuals reaching up to 47 cm ML (Rosenberg et al., 1981; Wiborg et al., 1982; Arkhipkin et al., 1999; Lordan et al., 2001b; Quetglas and Morales-Nin, 2004; Potoschi et al., 2009). 16.4.3 Maturation and reproduction Females generally outnumber males in catches outside the breeding areas because they are larger and faster and can migrate farther to forage. Borges and Wallace (1993) found that the average percentage of males in samples from Norway ranged from 4 to 18%, as compared with 3– 29% in Scotland. Quetglas et al. (1998b) found that males were significantly more abundant than females during winter in the western Mediterranean. Ripe males are present during most of the year in the southernmost areas of the Northeast Atlantic and the western Mediterranean (Quetglas et al., 1998b; Nigmatullin et al., 2002). In the northernmost regions of the species’ distribution, male maturity precedes that of females (Piatkowski et al., 1998; Lordan et al., 2001b). Differences observed in age and size at maturity (Table 16.2) between different geographic areas suggest that southern populations reach maturity and decrease somatic growth at younger ages and smaller sizes than northern ones, which attain larger sizes as a result of maintaining fast growth and delaying maturation (Arkhipkin et al., 1999; Quetglas and Morales-Nin, 2004). Table 16.2. Todarodes sagittatus. Minimum size of mature females and males (with values of MLm50%, when known, in parentheses) in populations from different geographic areas. Region ML (mm) Reference Females Males Off Norway 350 300 Wiborg et al. (1982) Northeast Atlantic 310 (~480) 280 (340) Lordan et al. (2001b) Northwest African waters 200 170 Arkhipkin et al. (1999) Western Mediterranean 318 (337) 196 (232) Quetglas et al. (1998b) Spawning probably takes place on the continental slope in late winter or early spring off northern Europe, in March and April off France, and between September and November in the western Mediterranean (Piatkowski et al., 1998; Quetglas et al., 1998b; Arkhipkin et al., 1999; Lordan et al., 2001b; Roper et al., 2010a). The main spawning grounds are probably situated on the Mid-Atlantic Ridge between the Azores and 45N (Sennikov et al., 1986). Cephalopod biology and fisheries in Europe: II. Species Accounts | 199 Potential fecundity (PF) estimates were considerably lower in squid from the Northeast Atlantic, ranging from 205 000 to 532 500 for females of 415–520 mm ML (Lordan et al., 2001b), than in mature females from the Sahara Bank (ML, 253–341 mm; PF, 215 000– 950 000) and in an immature female from the western Mediterranean (ML 288 mm; PF, 2 370 000) (Laptikhovsky and Nigmatullin, 1999). Spawning depth is 70–800 m off Portugal and >500 m in the western Mediterranean. 16.5 Biological distribution 16.5.1 Habitat Todarodes sagittatus may be found both in the open ocean and near the coast. It is known to migrate vertically between the surface at night and near-bottom waters by day (Mangold-Wirz 1963a; Clarke 1966; Korzun et al., 1979; Nesis, 1982/87; Vecchione et al., 2010); it can be found in surface waters above depths of 4595 m (Collins et al., 2001) and as deep (ROV observation) as 1947 m (Moiseev, 1991). 16.5.2 Migrations Todarodes sagittatus undertakes pronounced migrations, probably mainly related to feeding and spawning (Shimko, 1989). Foraging shoals of T. sagittatus have been reported from the Arctic since the late 1800s (see Golikov et al., 2013, for detail). Such excursions are described to last for long periods of time and to arise with a certain periodicity. Interestingly, these foraging shoals have not been recorded in Arctic waters between the early 1980s and recent years, apparently reappearing only in 2010 (Golikov et al., 2013). This finding is consistent with the highly unpredictable nature of the fishery (see below). From June on, large schools appear off the south and southwest coasts and in the northwestern fjords of Iceland and off the Faroe Islands, Norway, and, in some years, Scotland, where they stay until ca. December (Stephen 1937; Wiborg 1972, 1979a, 1987; Sundet, 1985; Joy, 1990; Boyle et al., 1998; Jonsson, 1998; Lordan et al., 2001b; Bjørke and Gjøsæter, 2004; Roper et al., 2010). In early winter, the animals migrate into deeper offshore water. On the fishing grounds around Madeira and other parts of the eastern Central Atlantic, the species is found in large numbers only between March and May (Borges and Wallace, 1993; Piatkowski et al., 1998; Arkhipkin et al., 1999; Lordan et al., 2001b). In the Mediterranean, a similar migration pattern is suggested by the higher catch per unit effort observed during July–August in the artisanal handjig fishery in the southern Tyrrhenian Sea (Potoschi and Longo, 2009) and the relatively more frequent occurrence noted in trawl catches during summer and autumn in the eastern basin (Katsanevakis et al., 2008). 16.6 Trophic ecology 16.6.1 Prey The diet of T. sagittatus consists mainly of fish, crustaceans, cephalopods, and polychaete worms, usually in the above-mentioned order of importance; cannibalism has also been noted by several authors (Table 16.3). In the eastern Atlantic, T. sagittatus feeds primarily on small mesopelagic fish such as pearlside and lanternfish, as well as on small gadoids and herring (Breiby and Jobling, 1985; Hernández-García, 1992; Lordan et al., 2001b), whereas in the western Mediterranean, silver scabbardfish appear to be the preferred prey species (Marabello et al., 1996; Quetglas et al., 1999). The prey spectrum found in different size classes reflects both increased body size and the ontogenetic migration of the species to deeper water (Quetglas et al., 1999; Lordan et al., 200 | ICES Cooperative Research Report No. 325 2001b). Differences are also reported between the diets of males and females (Wiborg et al., 1982; Quetglas et al., 1999). Table 16.3. Prey composition of Todarodes sagittatus, as known from studies in different regions of the eastern Atlantic and the western Mediterranean (compiled from Wiborg et al., 19821, Breiby and Jobling, 19852; Joy, 19903; Hernández-García, 19924; Marabello et al., 19965; Stowasser, 19976, 20047; Piatkowski et al., 19988; Quetglas et al., 19999; Lordan et al., 2001b10). Taxon Species Osteichthyes Acropomatidae Synagrops microlepis (thinlip splitfish)4 Alepisauridae Alepisaurus ferox (lancerfish)10 Ammodytidae Ammodytes tobianus (sandeel)1,2, Ammodytes spp.6,7 Argentinidae Argentina sphyraena (lesser argentine)1, Argentina spp.10, Glossanodon leioglossus (smalltoothed argentine)9 Belonidae Belone belone (garfish)10 Caproidae Capros aper(boarfish)4,8, Carangidae Trachurus trachurus (Atlantic horse mackerel)10 Centracanthidae Centracanthus cirrus(curled picarel)9, Spicara smaris (picarel)9 Chauliodontidae Chauliodus sloani (Sloane's viperfish)5 Clupeidae Clupea harengus (Atlantic herring)1,2,10, Sprattus sprattus6, indet.6,9 Epigonidae Epigonus telescopus (black cardinal fish)8 Gadidae Gadiculus argenteus(silvery pout)10, Gadus morhua (Atlantic cod)2, Melanogrammus aeglefinus (haddock)2,6,7, Merlangius merlangus (whiting)3,10, Micromesistius poutassou (blue whiting)1,2,6,7,10, Pollachius virens (saithe)2, Trisopterus esmarkii (Norway pout)1,2,3, Trisopterus minutus (poor cod)6, Trisopterus spp.6,10, indet.6,7 Macrouridae Macrourinae indet.8, Nezumia aequalis (common Atlantic grenadier)9, indet.4 Merlucciidae Merluccius merluccius (European hake)9 Myctophidae Benthosema glaciale (glacier lantern fish)1,9,10, Ceratoscopelus maderensis (Madeira lanternfish)9, Diaphus dumerilii4, Diaphus raffinesquii5, Diaphus spp.4,10, Hygophum benoiti (Benoit’s lanternfish)5, Hygophum hygomii (Bermuda lantern fish)9, Lampanyctus crocodilus (jewel lanternfish)5,9, Myctophum punctatum (spotted lanternfish)5,10, Notoscopelus elongatus9, Symbolophorus veranyi (large-scale lanternfish)9, indet.4,7,8,10 Moridae Lepidion lepidion (Mediterranean codling)9, Mora moro (common mora)9 Notacanthidae Polyacanthonotus rissoanus (smallmouth spiny eel)9 Osmeridae Mallotus villosus (capelin)2 Paralepididae Arctozenus risso (spotted barracundina)1,9, Paralepis spp.10, Sudis hyalina5, indet.5 Phosichthyidae Ichthyococcus ovatus5, Vinciguerria poweriae (Power's deepwater bristle-mouth fish)5, Vinciguerria attenuata5 Scombridae Scomber scombrus (Atlantic mackerel)10 Sebastidae Sebastes spp.1,2 Soleidae Microchirus boscanion (Lusitanian sole)8 Cephalopod biology and fisheries in Europe: II. Species Accounts Sparidae Sternoptychidae | 201 Boops boops (bogue)9 Argyropelecus hemigymnus (half-naked hatchetfish)5,9,10, Maurolicus muelleri (pearlside)1,2,5,7,9,10 Stichaeidae Leptoclinus maculatus (daubed shanny)2 Stomiidae Chauliodus sloani (Sloane's viperfish)9, Stomias boa (boa dragonfish)5,9 Trichiuridae Lepidopus caudatus (silver scabbardfish)9 Chondrichthyes Scyliorhinidae Galeus melastomus (black-mouthed dogfish)9, indet.9 Crustacea Decapoda Dendrobranchi- Aristeus antennatus9, Penaidea indet.4 ata-Penaeiodea Macrura reptantia- Nephrops norvegicus (Norway lobster)9, indet.4 Astacidea Pleocyemata- Galatheidae indet.8, Munida iris9, Munida spp.4,9 Anomura Pleocyemata-Car- Alpheus glaber9, Crangonidae indet.9, Oplophoridae indet.4, idea Pasiphaea multidentata9, P. sivado4,9, Pasiphaea spp.2,9,10, Plesionika giglioli9, P. heterocarpus4,9, Plesionika spp.4,8,9, Processa canaliculata9, Processa spp.9, indet.8 Euphausiacea Meganyctiphanes norvegica2, indet.8,10 Amphipoda Lyssianassidae indet.6, Parathemisto spp.1,10, Phrosina semilunata5, Phronima spp.5, Themisto abyssorum (as Parathemisto abyssorum)2, indet.1,3,10 Isopoda Cirolana sp.5, Idothea spp.1, indet.1,9 Copepoda Calanoidea indet.2, Pareuchaeta spp.1, indet.1,3,6,7,10 Cephalopoda Indet.9 Myopsida Loligo forbesii9, Loliginidae indet.5,7 Oegopsida Abralia veranyi (eye-flash squid)8, Abraliopsis spp.4, Ancistroteuthis lichtensteini (angel squid)9, Brachioteuthis riisei8, Cranchiidae indet.4,8 , Histioteuthis bonnellii (umbrella squid)5,9, H. reversa (elongate jewel squid)9, Gonatus spp.1,10, Illex coindetii (broadtail shortfin squid)9,10, Ommastrephidae indet.4,6,7,8, Onychoteuthis banksii (common clubhook squid)5,9, Onychoteuthidae indet.4, Thysanoteuthis rhombus(diamond squid)9, Todarodes sagittatus(European flying squid)1,2,5,9,10, Todaropsis eblanae (lesser flying squid)8, indet.8 Sepioidea Heteroteuthis dispar (odd bobtail)9, Neorossia caroli (carol bobtail)9, Sepia orbignyana4, Sepia spp.4,8, Sepietta neglecta9, Sepiola atlantica3, Sepiolidae indet.7,9 Octopoda Bathypolypus sponsalis (globose octopus)9, Eledone cirrhosa (horned octopus)6, Octopodidae indet.6 Gastropoda Thecosomata indet.7 Limacina retroversa (retrovert pteropod)2,10 Bivalvia indet.7 Polychaeta indet.3 Eunicida Eunice spp.2 Phyllodocida Nereis pelagica (bristlerworm)2,10, Nereis spp.1, 202 | ICES Cooperative Research Report No. 325 Chaetognatha Sagittoidea 16.6.2 Parasagitta elegans (as Sagitta elegans)2, Sagitta spp.1,2 Predators Todarodes sagittatus is an important prey item of many marine top predators. In the Northeast Atlantic and Mediterranean, its beaks have been found in the stomachs of cetaceans, seals, and fish (Table 16.4). Table 16.4. Known predators of Todarodes sagittatus in the Mediterranean Sea and Northeast Atlantic. Taxon Species Reference Chondrichthyes Black-mouthed dogfish (Galeus Carrasson et al. (1992), Villanueva melastomus) (1992), Bello (1996), Kabasakal (2002), Valls et al. (2011) Blue shark (Prionace glauca) Macnaughton et al. (1998) Cuckoo ray (Leucoraja naevus) Farias et al. (2006) Greater lantern shark Jakobsdottir (2001) (Etmopterus princeps) Portuguese dogfish (Cen- Clarke and Merrett (1972), Carrasson troscymnus coelolepis) et al. (1992) Shortfin mako (Isurus oxyrinchus) Maia et al. (2006) Smooth lanternshark Xavier et al. (2012) (Etmopterus pusillus) Osteichthyes Albacore (Thunnus alalunga) Bello (1999), Salman and Karakulak (2009), Romeo et al. (2012), Goñi et al. (2011) Alfonsino (Beryx splendens) Dürr and González (2002) Atlantic bluefin tuna (Thunnus Karakulak et al. (2009), Logan et al., thynnus) (2011), Romeo et al. (2012), Battaglia et al. (2013) Cod (Gadus morhua) Zuev and Nesis (1971) Common dolphinfish (Cory- Massutí et al. (1998) phaena hippurus) European hake (Merluccius Guichet (1995) merluccius) Greenland halibut (Reinhardtius Hovde et al. (2002) hippoglossoides) Lancetfish (Alepisaurus sp.) Zuev and Nesis (1971) Mediterranean spearfish (Te- Romeo et al. (2012) trapturus belone) Roundnose grenadier (Cory- Bergstad et al. (2010) phaenoides rupestris) Saithe (Pollachius virens) Zuev and Nesis (1971) Swordfish (Xiphias gladius) Bello (1985, 1991b, 1996), Guerra et al. (1993), Clarke et al. (1995), Hernández-García (1995), Ribeiro and Andrade (2000), Peristeraki et al. (2003, 2005), Salman (2004), Chancollon et al. (2006), Romeo et al. (2012) Cephalopod biology and fisheries in Europe: II. Species Accounts Aves Barolo shearwater (Puffinus bar- | 203 Neves et al. (2012) oli) Pinnipedia Harbour seal (Phoca vitulina) Bjørge et al. (1981) Harp seal (Pagophylus groen- Hauksson and Bogason (1995) landicus) Cetacea Bottlenose dolphin (Tursiops Orsi Relini et al. (1994), González et al. truncatus) (1994a), Blanco et al. (2001), Santos et al. (2001a, 2005a) Common dolphin (Delphinus Orsi Relini and Relini (1993), González delphis) et al. (1994a), Santos et al. (2013) Cuvier’s beaked whale (Ziphius Blanco et al. (1997), Lefkaditou and cavirostris) Poulopoulos (1998), Blanco and Raga (2000), Santos et al. (2001d), Spitz et al. (2011) Long-finned pilot whale (Globi- Orsi Relini and Garibaldi (1992), Spitz cephala melas) et al. (2011) Northern bottlenose whale (Hy- Clarke and Kristensen (1980), Santos peroodon ampullatus) et al. (2001c) Pygmy sperm whale (Kogia Spitz et al. (2011) breviceps) Risso’s dolphin (Grampus Clarke and Pascoe (1985), Bello griseus) (1992b, 1996), Carlini et al. (1992), Würtz et al. (1992b), Bearzi et al. (2011) Short-finned pilot whale (Globi- Hernández-García and Martín (1994) cephala macrorhynchus) Sperm whale (Physeter macro- Clarke and MacLeod (1976), Clarke cephalus) et al. (1993), Clarke and Pascoe (1997), Santos et al. (1999, 2002), Simon et al. (2003), Spitz et al. (2011) 16.7 Striped dolphin (Stenella co- Bello (1992c), Würtz and Marrale eruleoalba) (1993), Blanco et al. (1995) Other ecological aspects 16.7.1 Parasites Todarodes sagittatus is an important parasite host, representing a trophic bridge for parasite flow within marine ecosystems (Smith, 1984; Abollo et al., 1998; Gestal et al., 2000). Parasites recorded include the protozoan Aggregata sagitatta; the cestodes Phyllobothrium dohrni, P. sp., Nybelinia lingualis, and Amphistoma loliginis; the nematode Anisakis simplex B; and probably dicyemids (Zuev and Nesis, 1971; Pascual et al., 1996a; Gestal et al., 2000; González et al., 2003). 16.7.2 Environmental effects The abundance of T. sagittatus on the European shelf increases in colder years, the opposite situation to that of T. eblanae (Hastie et al., 1994). However, the relationships between its distribution and environmental factors, such as temperature and hydrological regimes, are still largely unknown (Golikov et al., 2013). Strandings on the beaches of the Strait of Messina (central Mediterranean) are probably related to unusual conditions such as a shift in currents (Berdar and Cavallaro, 1975). 204 | 16.8 ICES Cooperative Research Report No. 325 Fisheries Common fishing methods include jigging off Norway (Sundet, 1985) and artisanal hand-jigging in parts of the Mediterranean (Ragonese and Bianchini, 1990; Potoschi and Longo, 2009; Battaglia et al., 2010) and Canary Islands (Escánez Pérez et al., 2012), where there are directed artisanal fisheries. Over much of its distribution, it is taken mainly as bycatch in trawl fisheries (Joy, 1990; Jonsson, 1998; Lordan et al., 2001b; González and Sánchez, 2002). In several areas T. sagittatus caught by bottom trawling are either discarded (Sartor et al., 1998a; Machias et al., 2001) or sold cheaply as line bait (Thomas, 1973, as cited in Arnold, 1979). Indeed, Stroud (1978) noted that T. sagittatus was discarded by UK fishers when caught in the Northeast Atlantic and was probably an important underutilized species that could provide raw material for squid products. In general, the quality of fishery data is poor; data are not fully reported, and the various ommastrephid squids are often not separated. Todarodes sagittatus is reported as a separate category in FAO statistics (FAO, 2011), but such data have to be considered with caution. This is particularly true for the Mediterranean, where there has been confusion in the past about species reported in the FAO database under the general category “ommastrephids“, because other species, such as I. coindetii and T. eblanae, have been recorded as T. sagittatus (P. Jereb, pers. comm.). Also, there are discrepancies between and within the current available fishery statistics databases (i.e. the older FISHSTAT Plus and the more recent FISHSTAT J; FAO 2011), in relation to landings of this species. As is typical of ommastrephids, there can be wide fluctuations in catches between years, and recruitment to the fishery is probably highly variable. Mantle length of the exploited population ranges from ca. 20 to 40 cm (Norway) and from ca. 14 to 34 cm (Canary Islands). The body mass of fished specimens ranges from 150 g to 4 kg. Recruitment to the fishery begins at ca. 3 months of age. As with all European squid fisheries, there is currently no routine stock assessment for T. sagittatus. An important fishery for the species has existed intermittently off Norway. Fishing is concentrated during the months August–December in ICES Division IIa. FAO data (FAO, 2011) show that, since 1950, reported landings from this fishery were zero in several years, but there were occasional years of big landings, e.g. ca. 10 000 t in 1958 and 1965. The peak years of the fishery were during 1981–1985, with more than 18 000 t landed annually in both 1982 and 1983, but by 1989, annual landings had dropped to a mere 5 t, and the fishery effectively disappeared (see Wiborg, 1972, 1979a, 1987; Besteiro, 1985; Sundet, 1985; Bjørke and Gjøsæter, 2004; FAO, 2011). During the peak of the Norwegian fishery, the species was also frequently caught by trawlers based in Shetland (UK) (Joy, 1989, 1990). In some Mediterranean countries, the commercial value of T. sagittatus is relatively high. The main directed fishery operates in Italian waters, particularly in the Aeolian Islands (southern Tyrrhenian Sea). It is an artisanal handjig fishery in which fishers use handjig lines with a small blinking light. Fishers can achieve a catch per unit effort of 8.35 ± 2.55 kg d–1, with total catches reaching ca. 3000 t year–1, assuring a good income (Battaglia et al., 2010). In most areas, however, hand-jigging for T. sagittatus is practiced by professional and sport fishers only during late summer (Escánez Pérez et al. 2012; E. Lefkaditou, pers. comm.). Cephalopod biology and fisheries in Europe: II. Species Accounts | 205 Todarodes sagittatus is consumed fresh or boiled, although the flesh of large individuals has been described as tough. It is also marketed frozen, salted, or dried and is used as bait in finfish fisheries. Apart from it being an active predator on commercially important finfish species, the species has occasionally been considered a nuisance because of its competition with finfish for baited hooks. According to Nigmatullin et al. (2002), based on a study of the biology and ecology, the T. sagittatus inhabiting the outer shelf and upper slope of Northwest African waters (between ca. 10 and 26°N) are an isolated population differing from those in the North Atlantic and the Mediterranean. That population has a 1-year life cycle and spawns year-round, with a winter peak. It is suggested that the Northwest African squids represent a separate stock unit for fishery–biological management purposes and even, probably, a separate systematic unit, species, or subspecies. However, Martina Roeleveld (pers. comm. to Vladimir Laptikhovsky), upon studying a sample of mature males and females from the African population, found no distinctive features that would allow morphological separation of these squids from the North Atlantic population. 16.9 Future research, needs, and outlook Biological information on this species remains sparse. Important questions for future studies concern stock identification, the location of spawning grounds, description of egg development and the juvenile phase, as well as the validation of daily growth increments in statoliths. Results of such studies could provide a basis for the prediction of the vast migrations undertaken by this species, which are vaguely described, but not yet understood. 206 | ICES Cooperative Research Report No. 325 Cephalopod biology and fisheries in European waters: species accounts Todaropsis eblanae Lesser flying squid Cephalopod biology and fisheries in Europe: II. Species Accounts 17 | 207 Todaropsis eblanae (Ball, 1841) Paola Belcari, Uwe Piatkowski, Karsten Zumholz, Paolo Sartor, Evgenia Lefkaditou, Graham J. Pierce, Lee C. Hastie, A. Louise Allcock and Patrizia Jereb Common names Toutenon souffleur (France), Θράψαλο [thrapsalo] (Greece), totano tozzo (Italy), pota costeira (Portugal), pota costera (Spain), lesser flying squid (UK) (Figure 17.1). Synonyms Loligo eblanae Ball, 1841, Ommastrephes eblanae (Ball, 1841), Sthenoteuthis eblanae (Ball, 1841), Todaropsis veranyi Girard, 1890. 17.1 Geographic distribution The lesser flying squid (Todaropis eblanae Ball, 1841), exhibits a disjunct geographic distribution, being found in the eastern Atlantic and the entire Mediterranean (Figure 17.2), and in the West Indian Ocean, West Pacific Ocean, and eastern and northwestern Austalian waters (Roper et al., 2010a). In the eastern Atlantic, it has been recorded from the Shetland Islands and northeastern Scotland (e.g. Grimpe, 1921 in Grimpe, 1925; Stephen, 1944) down to South Africa (Roeleveld, 1998), where it is reported off Cape Town and the Cape of Good Hope (see references in Adam, 1952). However, very recent findings extend its distribution north to the Arctic, where it has been recorded since 2006 at distances >2500 km outside its previously documented range (Golikov et al., 2013). Figure 17.1. Todaropsis eblanae. Dorsal view. From Guerra (1992). Todaropsis eblanae is present in the North Sea, Skagerrak, and Kattegat (Grimpe, 1925; Jaeckel, 1958; Hornbörg, 2005; Zumholtz and Piatkowski, 2005), with occasional incursions into the northern North Sea (Stephen, 1944; Hastie et al., 1994) and off the east and west coasts of Ireland (Massy, 1928; Lordan et al., 1995). It is particularly abundant off the southwest coast of Ireland and in the Celtic Sea (Lordan et al., 2001a). It is widely distributed off the French, Spanish, and Portuguese coasts (Bouxin and Legendre, 1936; González et al., 1994b; Robin et al., 2002; Moreno et al., 2009), and down to West Africa (Hernández-García, 1991) and farther south. It is also distributed throughout the Mediterranean (Mangold and Boletzky, 1987; Bello, 2004; Salman, 2009), including western and central Mediterranean parts (Mangold-Wirz, 1963a; Sánchez, 1986a; Belcari and Sartor, 1993; Jereb and Ragonese, 1994; Giordano and Carbonara, 1999; Relini et al., 2002; Cuccu et al., 2003a), the Adriatic Sea (Casali et al., 1998; Krstulović Šifner et al., 2005, 2011; Piccinetti et al., 2012), the Ionian Sea (Tursi and D’Onghia, 1992; Lefkaditou et al., 2003a; Krstulović Šifner et al., 2005), the Aegean Sea, and the Levant Basin 208 | ICES Cooperative Research Report No. 325 (D’Onghia et al., 1992; Salman et al., 1997, 2002; Lefkaditou et al., 2003b). It has also been recorded in the Sea of Marmara (Katağan et al., 1993). Figure 17.2. Todaropsis eblanae. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 17.2 Taxonomy 17.2.1 Systematics Coleoidea – Decapodiformes – Oegopsida – Ommastrephidae – Todarodinae – Todaropsis. 17.2.2 Type locality Dublin Bay, Ireland. 17.2.3 Type repository Natural History Museum, National Museum of Ireland, Merrion St Upper, Dublin 2. Holotype [fide Hoyle (1903)]. 17.3 Diagnosis 17.3.1 Paralarvae No description of the paralarva (rhynchoteuthion) is yet available. Taxonomic characters permitting distinction of T. eblanae parlarvae from those of co-familiar species have been investigated very recently, based on in vitro fertilization experiments (Petroni et al., 2012). The skin sculpture of the external mantle surface, bearing a network of hexagonal cells, absent in Illex coindetii, seems the most promising character for the distinction of fresh rhynchoteuthions of T. eblanae from those of I. coindetii. Cephalopod biology and fisheries in Europe: II. Species Accounts 17.3.2 | 209 Juveniles and adults Adult external mophology is illustrated in Figure 17.3. Fin length is <50% of dorsal mantle length (ML), and fin width ranges between 75 and 90% of ML. Fins are rhomboid, with the anterior border more convex than the posterior border. Mantle width is >33% of ML. The head is wide and robust, with four nuchal folds in the neck region. The funnel groove lacks a foveola and side pockets. The funnel-locking cartilage is inverse T-shaped. The arms bear two longitudinal series of suckers. Sucker rings of the largest arm suckers bear one large pointed median tooth and 3–4 smaller pointed teeth (Figure 17.4a). The dactylus of the tentacular club (Figure 17.4b) bears four longitudinal series of small suckers. The manus of the club bears six transverse rows of four suckers, each with median pairs up to fourfold larger in diameter than the lateral suckers. Sucker rings of largest median club suckers are armed with ca. 30 short, pointed teeth, occasionally alternating with much smaller teeth (Figure 17.4a). Figure 17.3. Todaropsis eblanae. Dorsal (left) and ventral (right) views. Photos: Domenico Capua. (a) (b) Figure 17.4. Todaropsis eblanae. (a) Sucker rings of arm (left) and tentacle (right). Photo: Evgenia Lefkaditou. (b) Detail of the tentacular club. Photo: Domenico Capua. Left and right ventral arms (IV) of mature males are hectocotylized (Figure 17.5) by modification of suckers into cirrate lappets with transverse lamellae and an expanded protective membrane (Roper et al. 1984; Guerra, 1992; Roper et al., 2010a). Upper and lower beaks are illustrated in Figure 17.6. 210 | ICES Cooperative Research Report No. 325 (a) (b) Figure 17.5. Todaropsis eblanae. (a) Hectocotylized ventral arms of male. Photo: Domenico Capua. (b) Detail of hectocotylized arm (right IV) base with transverse lamellae. Photo: Evgenia Lefkaditou. Figure 17.6. Todaropsis eblanae. Lower beak (left) and upper beak (right). Photos: Evgenia Lefkaditou. 17.4 Life history The life cycle of T. eblanae is probably annual, because estimated values for the lifespan range from 7–8 months to 1 year. Spawning is year-round, with different seasonal peaks in different geographic areas. 17.4.1 Egg and juvenile development No records have been published on eggs in the wild. It is presumed that the species spawns pelagic egg masses, similar to many of its relatives within the family Ommastrephidae. Oocyte size in mature females varies between 0.8 and 2.5 mm along the principal axis throughout the species' range, with a mean of 1.2 mm in West African waters (Laptikhovsky and Nigmatullin, 1999) and in the Mediterranean (MangoldWirz, 1963a) and a mean of 1.57 mm in Scottish waters (Hastie et al., 1994). The duration of embryological development is unknown. The hatching season extends from October to March in British waters (Hastie et al., 1994; Collins et al., 2002) and from March to July, with a peak in May, in Northwest African waters (Laptikhovsky and Nigmatullin, 1999). 17.4.2 Growth and lifespan Maximum mantle lengths have been registered in North Atlantic waters: 290 and 220 mm for females and males, respectively (Robin et al., 2002). There is morphometric sexual dimorphism, with females attaining larger size than males (Mangold-Wirz, 1963a) (see Table 17.1). Cephalopod biology and fisheries in Europe: II. Species Accounts | 211 Table 17.1. Todaropsis eblanae. Maximum mantle length (mm) for females (F) and males (M) in different geographic areas of the eastern Atlantic and Mediterranean Sea. Region ML (mm) Reference F M Scottish waters 205 141 Hastie et al. (1994) North Sea 190 160 Zumholz and Piatkowski (2005) Bay of Biscay – Celtic Sea 290 220 Robin et al. (2002) Northwestern Spain 219 169 González et al. (1994b) Northwest Africa (16–26°N) 250 200 Arkhipkin and Laptikhovsky (2000) Northwest Africa (3–35°N) 215 164 Hernández-García (2002a) Western Mediterranean 204 156 Mangold-Wirz (1963a) Eastern Mediterranean 170 143 Zikos (2006), Lefkaditou (2006) Significant differences between sexes have been found in length–weight relationships in most of the studied regions (Table 17.2). In general, the values of the regression coefficient b are lower than 3 in both sexes. Table 17.2. Todaropsis eblanae. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations were converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a b Sex Reference Scottish waters 0.126 2.723 F Hastie et al. (1994) 0.115 2.777 M 0.142 2.660 F 0.094 2.854 M 0.330 2.41 F 0.670 2.15 M 0.148 2.671 F 0.088 2.917 M 0.0004 2.620 F 0.0003 2.687 M 0.224 2.505 All North Sea Bay of Biscay – Celtic Zumholz and Piatkowski (2005) Robin et al. (2002) Sea Northwestern Spain Portuguese waters Northwest African waters González et al. (1994b) J. Pereira, pers. comm. Arkhipkin and Laptikhovsky (2000) South African waters 0.110 2.67 All Cooper (1979) Western Mediterranean 0.039– 2.43– F Belcari et al. (1999) Sea 0.246 3.16 0.163– 2.11– 0.680 2.64 0.141 2.704 Eastern Mediterranean M All E. Lefkaditou, pers. comm. Sea The most statolith increments counted has been 255 (Robin et al., 2002), suggesting a lifespan not exceeding 1 year. Growth rates calculated from monthly changes in average ML are 0.76 cm month–1 (95% CL 0.12–1.24) in males and 1.22 cm month–1 (1.18– 1.86) in females, compared with 1.86 cm month–1 in males and 3.41 cm month–1 in females based on statolith data (Robin et al., 2002). As with other cephalopods, it is likely 212 | ICES Cooperative Research Report No. 325 that asynchronous hatching and recruitment make it difficult to interpret changes in average ML in samples from consecutive months. Daily growth rate is faster in females (Table 17.3), and instantaneous relative growth rate decreases with increasing size in both sexes (Arkhipkin and Laptikhovsky, 2000). Table 17.3. Todaropsis eblanae. Daily growth rate (DGR, mm d–1) and lifespan (months) of females (F) and males (M) in populations from the eastern Atlantic and Mediterranean Sea. (DA = direct ageing, MPA = modal progression analysis) Method DA DGR Lifespan F M F M 1.14 0.62 8.5 7.7 Region Reference Southern Celtic Robin et al. Sea – Bay of Bis- (2002) cay DA 0.7– 0.85– 1.8 1.6 0.41 0.25 Northwest Africa Arkhipkin and Laptikhovsky (2000) MPA 8.5 Southern Celtic Robin et al. Sea – Bay of Bis- (2002) cay MPA 17.4.3 0.2 0.15 Western Mediter- Mangold-Wirz ranean (1963a) Maturation and reproduction Most authors report that the sex ratio of T. eblanae is not substantially different from 1:1. Arkhipkin and Laptikhovsky (2000) found that the sex ratio was ca. 1:1 in winter and summer off Northwest Africa, but that there was a slight predominance of females in autumn (1.2:1). However, Zumholz and Piatkowski (2005) found an overall female:male ratio of 0.78:1 in research cruise catches in the North Sea. Given the existence of sexual dimorphism in size, these discrepancies might be caused by the use of sampling gears with different selectivities. Sexual maturation starts at a larger size in females than in males. Estimates of the size at maturity in different areas range from 120 to 150 mm ML for males and from 140 to 200 mm ML for females (Table 17.4) (Mangold-Wirz, 1963a; González et al., 1994b; Hastie et al., 1994; Joy, 1989; Arkhipkin and Laptikhovsky, 2000; Robin et al., 2002; Zumholz and Piatkowski, 2005). Mature females are reported to have particularly large nidamental glands, ranging from 7.5 to 27.7% of the total body weight in mature animals (Hastie et al., 1994). The spawning season probably extends throughout the year, with peaks varying according to geographic location (Belcari, 1999d). Todaropsis eblanae spawns mainly during summer and early autumn in the Catalan Sea (Mediterranean) (Mangold-Wirz 1963a) and in northern Atlantic waters (Hastie et al., 1994; Robin et al., 2002; Zumholz and Piatkowski, 2005; Oesterwind et al., 2010), whereas it spawns in early spring and early autumn in Atlantic waters south of 44°N (González et al., 1994b; Arkhipkin and Laptikhovsky, 2000). Cephalopod biology and fisheries in Europe: II. Species Accounts | 213 Table 17.4. Todaropsis eblanae. Minimum size at maturity and MLm50% (in parentheses) for females and males of populations from different geographical areas. Region ML (mm) Reference Females Males Scottish waters 110 (157.3) 92 (120.8) Hastie et al. (1994) North Sea 120 (164) 85 (123) Zumholz and Piatkowski (2005) Southern Celtic Sea – Bay (165) (135) Robin et al. (2002] 140 (180– 104 (130–149) González et al. (1994b) 120 Arkhipkin and Laptikhov- of Biscay Northwestern Spain 199) Northwest Africa (16–26°N) 150 sky (2000) Northwest Africa (3–35°N) 128 (168) 109 (130) Hernández-García (2002a) Western Mediterranean 160 110 Mangold-Wirz (1963a) The spawning grounds are still unknown. However, a possible location was identified in Northwest Iberian waters, where paralarvae matching the spawning season of T. eblanae were collected during plankton cruises in many years (Rocha et al., 1999; Moreno et al., 2009). Potential fecundity (PF) varies from 4500 to 28 000 for mature females in Scottish waters (Hastie et al., 1994), from 99 979 to 143 792 for females of 136–196 mm ML caught off Northwestern Spain (Rasero et al., 1995), and from 43 000 to 275 000 off West Africa (Laptikhovsky and Nigmatullin, 1999). Actual fecundity has been estimated in a number of ways. The number of ripe oocytes in the oviduct ranges from 5000 to 10 000 eggs in the western Mediterranean (Mangold-Wirz, 1963a), the number of mature (orange) eggs ranges from 355 to 13 157 in Scottish waters (Hastie et al., 1994), and the number of eggs in the oviducts ranges from 3600 to 34 400 off Northwest Africa (Laptikhovsky and Nigmatullin, 1999). For Galician waters, Rasero et al. (1995) report an average of 12 167 oocytes in the oviducts. Trends in both PF and numbers of ripe oocytes suggest a trend of decreasing egg numbers with increasing latitude, at least in the Atlantic. However, eggs from T. eblanae captured in Scottish waters are larger than from those captured in the Mediterranean and off West Africa (1.6 vs. 1.22 mm) (Laptikhovsky and Nigmatullin, 1999), suggesting that total reproductive output may be similar in northern and southern areas. The species can be considered an intermittent terminal spawner. Spent females are rarely found. The average number of spermatophores in the Needham’s sac is ca. 100, with a maximum of 269 in Northwest African waters (Hernández-García, 2002a; Sabirov et al., 2012) and 12–130 (mean = 60) in Scottish waters (Hastie et al., 1994). The number and length of spermatophores increases with the size of males. Males copulate several times, and spermatophores continue to be produced for further mating. 17.5 Biological distribution 17.5.1 Habitat Todaropsis eblanae is a demersal species associated with sandy and muddy bottoms, mainly in the lower sublittoral and upper bathyal over the continental shelf, usually not ascending to the surface or approaching the shore. It seems to live within a temperature range of 9–18°C and inhabits a wide range of depths (Guerra, 1992), being 214 | ICES Cooperative Research Report No. 325 more abundant in highly productive areas around the shelf break (Colloca et al., 2004). In the Mediterranean, it has been observed at depths of 200–600 m in the western area (Quetglas et al., 2000) and 30–700 m in Italian waters (Belcari and Sartor, 1993; Belcari, 1999d), but in the central basin and Hellenic seas, it has been recorded at 100–850 m and more frequently on the upper slope of regions with steep slopes (Krstulovic-Šifner et al., 2005; Lefkaditou, 2006; Katsanevakis et al., 2008). 17.5.2 Migrations Unlike other ommastrephid species, there is no evidence that T. eblanae regularly ascends to the surface or approaches shorelines (Hastie et al., 2009a; Oesterwind et al., 2010), although it is occasionally caught in coastal waters (Hastie et al., 1994). It is probably the least mobile of the ommastrephid squids in terms of migratory habits and is more likely to behave like neritic loliginid squid species than the sympatric ommastrephid species I. coindetii and Todarodes sagitattus (Lordan et al., 2001a; Roper et al., 2010a). 17.6 Trophic ecology 17.6.1 Prey The diet is composed, in decreasing order of importance, of fish, crustaceans, and cephalopods. Todaropsis eblanae is clearly an opportunistic predator, taking a wide variety of prey, particularly the most abundant in its habitat, e.g. blue whiting (Micromesistius potassou) made up nearly 50% of the diet off the Galician coast (Rasero et al., 1996) and Mueller's pearlside (Maurolicus muelleri) much of the diet off the southwest Irish coast (Lordan et al., 1998b). Cannibalism has been also recorded (Table 17.5). Table 17.5. Prey composition of Todaropsis eblanae, as known from studies in different regions of the Northeast Atlantic and the eastern Mediterranean (compiled from Hernández-García, 19921; Rasero et al., 19962; Lordan et al., 1998b3; Lelli et al., 20054; Vafidis et al., 20085). Taxon Species Osteichthyes Acropomatidae Synagrops microlepis (thinlip splitfish)1 Argentinidae Argentina sphyraena (argentine)2, Argentina spp.3, Glossanodon leioglossus (small-toothed argentine)4 Callionymidae Callionymus (dragonets) spp.2 Caproidae Capros aper (boarfish)4 Carangidae Trachurus trachurus (Atlantic horse mackerel)2,3 Cepolidae Cepola macrophthalma (red bandfish)2 Clupeidae Clupea harengus (Atlantic herring)3, Sprattus sprattus (European sprat)3, indet.3,4 Congridae Gadidae indet.4 Gadiculus argenteus (silvery pout)2,3,4, Micromesistius poutassou (blue whiting)2,3, Trisopterus spp.3, indet.2 Gobiidae Aphia minuta (transparent goby)2,3 , indet.2,3,4 Lotidae Gaidropsarus biscayensis (Mediterranean bigeye rockling)2, Lotinae indet. larvae3 Macrouridae indet.4 Merlucciidae Merluccius merluccius (European hake)2,3 Myctophidae Diaphus spp.1, indet.1 Cephalopod biology and fisheries in Europe: II. Species Accounts | 215 Pleuronectiformes indet.2 Sternoptychidae Maurolicus muelleri (pearlside)3,4 Crustacea Decapoda Dendrobranchiata- indet.1 Penaeiodea Macrura reptantia indet.2 Pleocyemata- Galatheidae indet.2, Munida spp.1, indet.1 Anomura Pleocyemata-Brachy- indet.2,5 ura Pleocyemata-Car- Dichelopandalus bonnieri3, Pandalidae indet.1, Pasiphaea si- idea vado1, Pasiphaea spp.1,2,3, Plesionika spp.1, indet.1 Euphausiacea Meganyctiphanes norvegica2,3, indet.3 Mysida indet.5 Amphipoda indet.4 Cephalopoda Myopsida Alloteuthis spp.2,4, Loligo forbesii3, Loligo spp.2 Oegopsida Abraliopsis spp.1, Illex coindetii2,3, Todaropsis eblanae2,3, Ommastrephidae indet.1,2 Octopoda Eledone cirrhosa2, indet.4 Sepioidea Sepietta oweniana4 Gastropoda Heliconoides inflatus4, Limacina retroversa3, indet.4 Bivalvia indet.4 17.6.2 Predators Toothed whales and dolphins are considered to be the most important predators of this species, but it is also preyed on by a wide variety of birds, fish and cephalopods (Roper et al., 1984, 2010a; Guerra, 1992; Table 17.6). Table 17.6. Known predators of Todaropsis eblanae in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Cephalopoda Clubhook squid (Onychoteuthis Hastie et al. (2009a) banksii) Chondrich- Black-mouthed dogfish (Galeus me- thyes lastomus) Kabasakal (2002) Blue shark (Prionace glauca) Clarke and Stevens (1974) Portuguese shark (Centroscymnus Hastie et al. (2009a) coelolepis) Shortfin mako shark (Isurus oxyrinchus) Hastie et al. (2009a) Sleeper shark (Somniosus spp.) Hastie et al. (2009a) Smooth hammerhead (Spyrna zi- Hastie et al. (2009a) gaena) Smooth lanternshark (Etmopterus pusil- Xavier et al. (2012) lus) Osteichthyes Albacore (Thunnus alalunga) Hastie et al. (2009a) 216 | ICES Cooperative Research Report No. 325 Atlantic bluefin tuna (Thunnus thynnus) Karakulak et al. (2009), Romeo et al. (2012) Swordfish (Xiphias gladius) Hernández-García (1995), Salman (2004), Hastie et al. (2009a) Aves Cetacea Great albatross (Diomedea spp.) Hastie et al. (2009a) Sooty albatross (Phoebetria fusca) Hastie et al. (2009a) Bottlenose dolphin (Tursiops truncatus) Santos et al. (1997, 2007), Blanco et al. (2001) Common dolphin (Delphinus delphis) Pascoe (1986) Northern bottlenose whale (Hyperoo- Santos et al. (2001c) don ampullatus) Risso’s dolphin (Grampus griseus) Clarke and Pascoe (1985), Bearzi et al. (2011), Bloch et al. (2012) Sperm whale (Physeter macrocepha- Hastie et al. (2009a) lus) 17.7 Spotted dolphin (Stenella attenuata) Hastie et al. (2009a) Striped dolphin (Stenella coeruleo- Würtz and Marrale (1993), alba) Blanco et al. (1995) Other ecological aspects 17.7.1 Parasites Todaropsis eblanae can host at least six species of helminth: three tetraphyllidean cestodes (Phyllobothrium sp., Pelichnibothrium speciosum, Dinobothrium sp.); two trypanorhynchidean cestodes (Nybelinia yamagutii, Nybelinia lingualis); and one ascaridoid nematode (Anisakis simplex) (Smith, 1984; Pascual et al., 1996a, b, c; 1999). Todaropsis eblanae is the most important paratenic host for Anisakis (Abollo et al., 1998, 2001), but it is only occasionally infected in regions of strong coastal upwelling (Pascual et al., 2007). Copepods (Pennella sp.) (Pascual et al., 1997) and isopods (Pascual et al., 2002) have also been recorded in this species. Additional studies on T. eblanae and I. coindetii parasites (Pascual et al., 1996b) suggest that these species are sympatric and share similar econiches and that parasites may also be useful as an indirect indicator of the migratory habits of the squid. 17.7.2 Environmental effects Abundance indices of T. eblanae derived from 21 cruises off northwestern Spain (30– 500 m depth) were significantly positively related with the upwelling index (Lavín et al., 1991) for this area (Rasero, 1994, 1996; Rocha et al., 1999). This relationship might be due to the increased survival rates of hatchlings and prerecruits when abundance of prey inceases as a consequence of greater productivity caused by seasonal upwelling. These conclusions are supported by results achieved from 57 plankton cruises carried out during a 19-year research programme in Iberian waters (Moreno et al., 2009). The species is scarce in the northern North Sea, although there may be occasional huge aggregations. These historical phenomena may be linked to hydrographical anomalies such as incursions of warm, high-salinity Atlantic seawater into the North Sea (Rae and Lamont, 1963; Hastie et al., 1994). Cephalopod biology and fisheries in Europe: II. Species Accounts | 217 The very recent findings of T. eblanae in the Arctic Sea described by Golikov et al. (2013) seem to be connected to the continuous warming of those waters as a consequence of climatic change recently. Todaropsis eblanae appears to have spread into the Barents Sea via the eastern branch of the Norwegian Current and farther by the southern branch of the North Cape coastal current as far as the Murman shelf (Golikov et al., 2013). 17.8 Fisheries Recruitment is year-round, with a peak in autumn–early winter (Rasero, 1996; Belcari, 1999d; Rocha et al., 1999; Robin et al., 2002). Todaropsis eblanae is taken throughout the year as bycatch in otter trawl fisheries, and, to a lesser extent, by gill- and trammelnets, longlines, and jigging at depths of 100–400 m in the Mediterranean, off West Africa, and in the Northeast Atlantic. Most catches are made at ca. 200 m in the North Atlantic (Robin et al., 2002) and at 200–800 m in Italian waters, with wide annual fluctuations in catches presumably reflecting high between-year variability in abundance (González et al., 1994b; Hastie et al., 1994; Belcari, 1999d). Few official fishery statistics are available for the species. Landings from the ICES Area and the Mediterranean are usually pooled for different ommastrephid squid species, including lesser flying squid (T. eblanae), broadtail shortfin squid (I. coindetii), European flying squid (T. sagittatus), and neon flying squid (Ommastrephes bartramii). However, the species has been identified in commercial landings in Ireland, UK, France, Spain, and Portugal in the North Atlantic, and in Spain, Italy, and Greece in the Mediterranean; some data on its landings are available from market sampling in France, Spain, and Portugal (Robin et al., 2002; Bruno, 2008; Bruno and Rasero, 2008; Bruno et al., 2009). Todaropsis eblanae is less important than I. coindetii in shortfin squid landings in France (Robin et al., 2002) and northern Spain (Bruno and Rasero, 2008). It does make up ca. 40% of ommastrephid landings along the Spanish Atlantic coast (Bruno and Rasero, 2008), although those authors reported both seasonal variation and differences between gears: T. eblanae made up 81% of pair-trawl ommastrephid landings. Further analysis by Bruno et al. (2009) showed that T. eblanae was relatively more common in ICES Division VIIIc-W than in Division IXa-N, i.e. it formed a greater proportion of landings farther north. Total landings of shortfin squids from the Mediterranean and Iberian Atlantic waters can be fairly consistent from year to year. The species is a minor component of the catch of the French fishery operating in the northern Bay of Biscay and Celtic Sea. Farther north, landings have generally been sporadic. At present, I. coindetii, O. bartramii and T. eblanae are not exploited commercially by UK fleets. However, reports from adjacent waters indicate that, at times, they can be widespread and abundant in the Northeast Atlantic and may represent a significant potential fishery resource (Hastie et al., 2009a). 17.9 Stock identity Results of molecular investigations suggest the presence of at least three genetically isolated populations across the species' distribution range in the eastern Atlantic (Dillane et al., 2005), a fact that has important implications for sustainability of the resource, although it is important to note that fishing on this species is not currently regulated and is unlikely to be managed in the immediate future. The substantial genetic differences existing among samples from European waters (Northeast Atlantic and Mediterranean), from Southeast Atlantic waters off Mauritania, and off South Africa may explain the geographic variation observed in the hectocotylized arm morphology, as well 218 | ICES Cooperative Research Report No. 325 as in spermatophore morphology among animals from the Atlantic and Indian oceans (Sabirov et al., 2012). The presence of the species in the Southwest Indian Ocean (Saya de Malha and Nazareth banks, Mascarene Ridges) was recorded by Korzun et al. (1979). It has also been reported in the South China Sea (Chen and Guo, 2001; Shevtsov and Katugin, 2006) and in Australian waters from the Timor Sea (Nesis, 1979a) down along the east and west coasts of Australia (Lu, 1982; Dunning, 1998; Wormuth, 1998). However, no data on the genetic identity of these populations are available to date. 17.10 Future research, needs, and outlook Important topics for future research include further investigation of intraspecific divergence of T. eblanae, stock separation, detection of spawning sites, and description of early life stages. Further studies on parasites could explore their use as indirect indicators of the species’ migratory habits (Pascual et al., 1996b). In addition, there is a need to study the effect of parasites on squid growth (Pascual et al., 2005). For assessment and management purposes, cephalopod species should be adequately identified in landings. It is also recommended that sampling of cephalopods in EU waters is stratified by métier and that sampling frequency and intensity are sufficient to follow the growth of different microcohorts. In addition, data on maturation and length composition by microcohort from research surveys should be analysed to assess trends in recruitment and length at 50% maturity (MLm50%). Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Ommastrephes bartramii Red flying squid | 219 220 | 18 ICES Cooperative Research Report No. 325 Ommastrephes bartramii (Lesueur, 1821) A. Louise Allcock, Patrizia Jereb, Evgenia Lefkaditou, Graham J. Pierce, Lee C. Hastie, and Uwe Piatkowski Common names Encornet volant, encornet carol (France); Θράψαλο [thrapsalo], Καταμάχι4 [katamachi] (Greece); totano, totano nero 4 (Italy); pota saltadora (Spain); potasaltadora, pota-de-orelhas (Portugal); neon flying squid, red flying squid (UK) (Figure 18.1). Synonyms Loligo bartramii Lesueur, 1821, Sthenoteuthis bartramii (Lesueur, 1821), Stenoteuthis bartrami (Lesueur, 1821), Loligo vitreus Rang, 1835 in Férussac and d'Orbigny, 1834–1848, Ommastrephes cylindraceus d'Orbigny, 1835 in 1834–1847, Onychoteuthis brevimanus Gould, 1852, Loligo pironneauii Souleyet, 1852, Loligo touchardii Souleyet, 1852, Ommastrephes caroli Furtado, 1887, Ommatostrephes caroli Furtado, 1887, Ommastrephes caroli stenodactyla Rancurel, 1976, Ommastrephes caroli stenobrachium Rancurel, 1976. 18.1 Geographic distribution Figure 18.1. Ommastrephes bartramii. Dorsal view. From Guerra (1992). The neon flying squid (Ommastrephes bartramii Lesueur, 1821) has a circumglobal, subtropical, and partly temperate distribution, but is excluded from the equatorial waters of all three major oceans (Roper et al., 2010a). It has the greatest geographic range of all ommastrephids (Dunning, 1998), although its distribution is discontinuous between the southern and northern hemispheres. In the South Pacific, it extends from Chile in the east to the Tasman Sea in the west (Polezhaev, 1986; Dunning, 1998). In the Southeast Indian Ocean, it has been reported from off Western Australia (Filippova, 1968, 1971) and from the Great Australian Bight (Nesis, 1979a). In the South Atlantic, it is found from 14 to 27°S off Africa (Roeleveld, 1998) and from 27 to at least 45°S off South America (Zuev et al., 1976; Roper et al., 1984), with recent coastal records from Argentina (Ré et al., 2002). In the North Pacific, O. bartramii is particularly abundant off the Pacific coast of Japan (Okutani et al., 1981). In the North Atlantic, O. bartramii ranges from the Caribbean coast of Central America, north to the Grand Banks, across the Atlantic as far north as Iceland, east to the British Isles and the western North Sea, as far south as Madeira, and into the Mediterranean (Clarke, 1966; Zuev and Nigmatullin, 1975) (Figure 18.2). Ommastrephes bartramii is widespread throughout the Mediterranean (Torchio, 1968; Bello, 1986, 2004; 4 Names used by fishers, not official names Cephalopod biology and fisheries in Europe: II. Species Accounts | 221 Salman, 2009; Lefkaditou et al., 2011), including western and central Mediterranean parts (Biagi, 1990; Orsi Relini, 1990; Ragonese and Jereb, 1990, Ragonese et al., 1992; Sanchez et al., 1998a; Cuccu et al., 2009c), the Gulf of Taranto (Torchio, 1967; Bello, 2007), the Adriatic Sea (Guescini and Manfrin, 1986b; Bello, 1990), the whole of the Aegean Sea (Akyol and Şen, 2004; Lefkaditou et al., 2011), and the Levantine Basin (Katağan et al., 1992; Lefkaditou et al., 2011). Lefkaditou et al. (2011) provides a list of the Mediterranean records to date. Figure 18.2. Ommastrephes bartramii. Geographic distribution in the Northeast Atlantic and Mediterranean Sea. 18.2 Taxonomy 18.2.1 Systematics Coleoidea – Decapodiformes – Oegopsida – Ommastrephidae – Ommastrephinae – Ommastrephes. 18.2.2 Type locality Type Locality not indicated. 18.2.3 Type repository Specimen no longer extant [fide Voss (1962) and Lu et al., 1995)]. Originally in Academy of Natural Sciences, 19th and The Parkway, Philadelphia, Pennsylvania, 19103, USA. 18.3 Diagnosis 18.3.1 Paralarvae Detailed descriptions of paralarvae from the Pacific are available (Okutani, 1968, 1969; Young and Hirota, 1990; Wormuth et al., 1992; Sakurai et al., 1995). The following diagnosis of Atlantic paralarvae is abbreviated from Nesis (1979b); see also Figure 18.3 below. The mantle is narrow, barrel-like in early larvae, cup-shaped or semi-fusiform 222 | ICES Cooperative Research Report No. 325 later. The head is narrow, not retracting into the mantle. Arms III develop at 1.5 mm, arms IV at 2.5–3 mm ML. The proboscis is narrow, slender, longer than the arms in early larvae; lateral suckers at the tip are larger than those in the middle; it splits when animals measure between 5 and 9 mm. Chromatophores are small, closely packed, brown and carmine in colour. Figure 18.3. Ommastrephes bartramii. Four-day-old hatchling off Hawaii. Photo: Yasunori Sakurai. 18.3.2 Juveniles and adults Dunning (1998) gives the following description: "Funnel groove with foveola and side pockets; tetraserial suckers on dactylus of tentacular club; medial manus-sucker rings with one tooth in each quadrant greatly enlarged; carpal-fixing apparatus consisting of smooth-ringed suckers and knobs on tentacular stalk; small, irregularly shaped, subcutaneous photophores present in adults, embedded in ventral mantle and ventrally in head; no photophores in paralarvae; either left or right arm IV hectocotylized by complete loss of suckers and sucker bases distally in mature males; mantle-funnel locking apparatus not fused." The tentacular clubs (Figure 18.4), suckers on arms and tentacular clubs (Figure 18.5), and beaks (Figure 18.6) are illustrated below. Figure 18.4. Ommastrephes bartramii. Tentacular club. Photo: Evgenia Lefkaditou. Cephalopod biology and fisheries in Europe: II. Species Accounts | 223 Figure 18.5. Ommastrephes bartramii. Sucker rings from arm (left) and tentacular club (right). Photos: Evgenia Lefkaditou. Figure 18.6. Ommastrephes bartramii. Lower beak (left) and upper beak (right). Photos: Evgenia Lefkaditou. 18.4 Remarks Nesis (1982/1987) considered that the southern hemisphere populations were likely to represent a separate subspecies, and that the North Atlantic and North Pacific populations, separated by the land barrier (the Americas), were also likely to merit subspecific status. Pinchukov (1975) also considers the North Atlantic and South Atlantic populations to be separate subspecies. Nesis (cited in Dunning 1998) suggested that a coldwater barrier prevents the mixing of the South Pacific and Indian Ocean populations, indicating that the Indian Ocean population might represent another subspecies. Nesis (1979a) also suggested that two populations may exist in the South Atlantic (separate eastern and western populations) and that two populations may exist in the Indian Ocean (again, separate eastern and western populations). However, Shevtsova et al. (1977) showed that the cholinesterases from squid from the Southeast Atlantic populations and the Great Australian Bight had identical properties, suggesting occasional genetic exchange between the populations. The cholinesterases of North Atlantic, North Pacific, and southern hemisphere squids all differed from each other (Shevtsova et al., 1979). A study also found differences in spermatophore morphology (Nigmatullin et al., 2003). The distribution of O. bartramii was believed neither to extend into the Mediterranean nor as far north as Iceland (Roper et al., 1984), its niche in these areas instead being occupied by Ommastrephes caroli. However, revisions of the Ommastrephidae by Zuev et al. (1975, 1976) and Nigmatullin (1979, 2007) determined that O. caroli was, in fact, a junior synonym of O. bartramii. Naef (1921/1923) specifically referred to this species as 224 | ICES Cooperative Research Report No. 325 “much more frequently found” on the market in Naples than Todarodes sagittatus; however, O. bartramii has long been considered uncommon in the Mediterranean, given the sporadic captures of isolated specimens (Torchio, 1967). Subsequent findings and records of young specimens suggest the species to be more common than sometimes suggested (Orsi Relini, 1990; Katağan et al., 1992; Ragonese et al., 1992; Bello, 2007), and recent observations suggest that the abundance of O. bartramii is currently increasing in the Mediterranean (see Lefkaditou et al., 2011, for a review). 18.5 Life history Ommastrephes bartramii is believed to live for ca. 1 year, with females reaching markedly larger size than males. Reproduction has a seasonal periodicity, which varies between areas across the distribution. 18.5.1 Egg and juvenile development There are few data available on development of O. bartramii from the North Atlantic. Naef (1921/1923) describes the development of ommastrephid embryos from egg masses found floating in surface waters near Naples that he considers are “highly likely” to be attributable to O. bartramii. He describes the formation of the typical rhynchoteuthis larva with tentacles fused into a ”proboscis”, which is characteristic of ommastrephids. Wormuth et al. (1992) suggest that Naef's egg masses are, in fact, probably attributable to Illex coindetii, and it is now thought that wild-spawned O. bartramii egg masses have never actually been seen. Detailed information on embryonic development through hatching was provided by artificial fertilization of Pacific stock. Eggs measured 0.9 × 1.1 mm; they hatch into rhynchoteuthis paralarvae (Sakurai et al., 1995). There are various estimates of hatchling size at proboscis separation. Splitting appears to begin at 4–5 mm ML (Shea, 2005), but estimates of size at completion of this process range from 7 (Wormuth et al., 1992) to 12 mm (Bigelow and Landgraf, 1993). Around this time, growth changes from an exponential to a linear pattern (Yatsu and Mori, 2000; Bigelow and Landgraf, 1993). Although the tentacles are still very underdeveloped at this stage (Shea, 2005), the change in growth patterns indicates a change in feeding habits, and this may correspond with the end of the paralarval stage (Anon., 2005). There are several records of rhynchoteuthis paralarvae from the North Atlantic (e.g. Rocha et al., 1999; Collins et al., 2002), but these are rarely identified to species (although see Diekmann and Piatkowski, 2002). Nigmatullin (1987) suggests that newly hatched Ommastrephes rhynchoteuthis paralarvae have a mantle length of ca. 1 mm. They inhabit the surface layers to depths of ca. 250 m (Zuev and Nesis, 1971). The best descriptions of paralarvae are from the Pacific (see above), where research is driven by the needs of the commercial fishery. The artificial fertilization technique developed by Sakurai et al. (1995) has led to paralarvae being readily available on board research vessels in the Pacific. 18.5.2 Growth and lifespan Ommastrephes bartramii females reach markedly larger size than males. Females also have narrower fins and larger suckers. Males reach a maximum mantle length of 45 cm, but two size groups of females can be distinguished: one maturing at 36–65 cm ML, and the other at >70 cm ML. In the North Atlantic, the maximum documented ML of a female is 90 cm (BW 25 kg) and of a male is 42 cm (BW 2.2 kg) (Nigmatullin, 1989). Around Madeira, females reach a maximum size of 69 cm ML and males a maximum size of 36 cm ML; Lefkaditou et al. (2011) give maximum sizes for the Mediterranean Cephalopod biology and fisheries in Europe: II. Species Accounts | 225 as 66 and 32 cm ML, respectively. Guerra et al. (2010b) listed a specimen of 102 cm ML and BW of ca. 35 kg captured in the eastern tropical Pacific. Research from the Pacific suggests that O. bartramii live for ca. 1 year (Yatsu et al., 1997; Yatsu, 2000). However, for larger females, lifespan is not known and may be longer. Most available information on length–weight relationships and growth refers to this species in the Pacific (e.g. Yatsu and Mori, 2000; Chen and Chiu, 2003). Growth of females is slightly more rapid than for males, as expected from the marked sexual dimorphism (Yatsu et al., 1997; Yatsu, 2000). There are again few available data on growth in European waters. Lefkaditou et al. (2011) report a length–weight relationship for the Mediterranean, based on a sample of 30 individuals of both sexes, using an exponential model, because this had a slightly higher r2 value than the traditional power equation. For consistency, we include the power equation version here: BW = 0.310 × ML3.044. The most comprehensive data are probably those of Pinchukov (1975), who studied maturation, fecundity, and horizontal migrations, sampling >400 O. bartramii from the North Atlantic and an additional 25 specimens from the Mediterranean. However, those data are in an unpublished Master of Arts thesis in Russian and were not available for this review. Nigmatullin (1987) summarizes the changes in body size and ecological niche as O. bartramii develops (Table 18.1). Table 18.1. Ecological changes in Ommastrephes bartramii with growth. Data from Nigmatullin (1987). Habitat Maturity Stage Size (mantle length) Food Plankton Egg mass 1 mm n/a Plankton Paralarva 1–8 mm Macroplankton Plankton Juvenile 1–2.5 cm Mesozooplankton Micronekton Juvenile 3–8 cm Macrozooplankton Nekton Subadult/adult >15 cm Fish and squid Rostral length of the lower beak (LRL) increases linearly with increasing mantle length (ML). In the Northeast Atlantic, this relationship is described by the equation ML = 8.55 + 40.72LRL (r2 = 0.98), based on 57 O. bartramii (59–590 mm ML). Lefkaditou et al. (2011) indicate that a power regression better fits data from the Mediterranean: ML = 36.2613 × LRL1.069 (r2 = 0.95, n = 11). 18.5.3 Maturation and reproduction Sexual maturation in the female begins when it reaches a length of ca. 40 cm ML. Females produce 3–8 million eggs or more (Nigmatullin and Laptikhovsky, 1994) ca. 1 mm long, which they are thought to lay in underwater floating ribbons (Hastie et al., 2009a). Reproduction takes place towards the end of summer and at the beginning of autumn. In the North Atlantic, two groups of females mature at different sizes: the middle-sized group is mature at 36–65 cm of ML and larger-sized group at >70 cm ML (Gaevskaeya and Nigmatullin, 1976; Nigmatullin, 1989). North Atlantic males start maturing at 27–30 cm ML, and all males >32 cm are mature. Spawning is throughout the year in the North Atlantic, with some seasonal activity from spring to the beginning of autumn (Gaevskaya and Nigmatullin, 1976; Roper et al., 2010a). In the North Pacific population, there are two cohorts, one that begins spawning in September, the other with a winter spawning season, with females beginning their spawning activity in November–December (Bower and Ichii, 2005). 226 | 18.6 ICES Cooperative Research Report No. 325 Biological distribution 18.6.1 Habitat Individuals of O. bartramii are rare in the North Sea and are thought only occasionally to pursue fish to this region. They perish in cold waters and may be found on the shore in The Netherlands following cold stormy weather (Zuev and Nesis, 1971); at least one specimen has been stranded as far north as Yorkshire in Great Britain (Robson, 1925). The greatest abundance of O. bartramii in the North Atlantic is thought to be in the Madeira-Azores–Canary Islands region (Zuev and Nigmatullin, 1975). Ommastrephes bartramii have been caught at 400–500 m over the Mid-Atlantic Ridge at 44–47°N (Khromov, 1987b) and at other ridge locations in the North Atlantic (Zuev et al., 1976). Despite the wide distribution of O. bartramii, reproduction appears to be limited to areas between 25 and 40°N and south of the equator, with foraging taking place elsewhere throughout its known range (Aleksandronetz et al., 1983). Zuev et al. (1976) suggest that it is limited to waters of 14–17°C. Shoals of O. bartramii rarely comprise more than 30 individuals (Zuev and Nigmatullin, 1975). At night, they appear to avoid areas where the water depth is exceptionally shallow directly above seamounts (review: Moiseev and Nigmatullin, 2002). 18.6.2 Migrations Individual O. bartramii have been observed from manned submersibles (Sever-2, TINRO-2, and Tethys) over the Mid-Atlantic Ridge and adjacent areas (including Croner Rise, Josephine Seamount, and the South Azores Seamount complex). They have been recorded near the surface at night (down to 100 m), and at 560–1050 m by day (Moiseev, 1987, 1991). They are believed to undergo diel vertical migrations of 1000–1500 m. Upward (night-time) migration is at speeds of up to 5 m m–1, with migrations taking between 30 min and 2.5 h, depending on the starting daylight depth (Moiseev, 2001). In the North Atlantic, shoals of larger squid, mainly females, make a feeding migration at the beginning of the summer to areas north of 40°N, including the North Sea and Newfoundland, and then return in autumn to lower latitudes to the reproductive part of their range (Zuev and Nigmatullin, 1975; Gaevskaya and Nigmatullin, 1976; Zuev et al., 1976). 18.7 Trophic ecology 18.7.1 Prey Ommastrephes bartramii takes mainly fish (especially myctophids, garfish, flying fish, and mackerel); squids, including its own species; crustaceans (amphipods, decapod larvae, euphausiids, and shrimps); and heteropods in the Northeast Atlantic (Table 18.2) and in other parts of its range, e.g. the Southwest Atlantic (Lipiński and Linkowski, 1988). Cephalopod biology and fisheries in Europe: II. Species Accounts | 227 Table 18.2. Prey composition of Ommastrephes bartramii, as known from studies in the Northeast Atlantic and eastern Mediterranean Sea (compiled from Zuev and Nesis, 19711; Ch. Nigmatullin, pers. comm. (based on Gaevskaya and Nigmatullin, 1976, and Nigmatullin and Pinchukov, 1976; both papers in Russian)2; Vafidis et al., 20083). Taxon Families and species Osteich- Beloniformes indet. (garfish, flying fish)1, Myctophidae indet. (lanternfish)1,2, Scombri- thyes dae indet. (mackerel)1, indet.1,2,3 Crusta- Decapoda indet. larvae 2, Euphausiacea indet.,2, Mysida indet.3, Amphipoda cea indet.2, Hyperiidae indet.2, Phronimidae indet.2, Copepoda indet.2 Cepha- Onychoteuthis banksii2, Enoploteuthidae indet.2, Oegopsida indet.1,2 , indet.3 lopoda Limacinidae indet. (pteropod)1, Pterotracheoidea indet.2 Gastropoda 18.7.2 Predators Ommastrephes bartramii is preyed upon by a variety of cetaceans, but also by large fish such as tuna and swordfish (Table 18.3). Table 18.3. Known predators of Ommastrephes bartramii in the Mediterranean Sea and Northeast Atlantic. Taxon Species References Chondrich- Portuguese dogfish (Centroscym- Carrasson et al. (1992) thyes nus coelolepis) Osteichthyes Albacore (Thunnus alalunga) Salman and Karakulak (2009) Atlantic bluefin tuna (Thunnus Battaglia et al. (2013), Romeo et al. thynnus) (2012) Swordfish (Xiphias gladius) Bello (1991b), Guerra et al. (1993), Hernández-García (1995), Salman (2004), Chancollon et al. (2006), Romeo et al. (2009, 2012) Cetacea Cuvier's beaked whale (Ziphius Carlini et al. (1992) cavirostris) False killer whale (Pseudorca cras- Hernández-García (2002b) sidens) Pygmy sperm whale (Kogia brevi- Martins et al. (1985) ceps) Sperm whale (Physeter macro- Clarke et al. (1993) cephalus) Risso's dolphin (Grampus griseus) 18.8 Bearzi et al. (2011) Other ecological aspects 18.8.1 Parasites Parasites of O. bartramii in the North Atlantic include two species of didymozoid trematode, larvae of three species of cestode, two species of nematode, and one acanthocephalan (Gaevskaya and Nigmatullin, 1976). The helminth fauna is identical in the South Atlantic, and Gaevskaya and Nigmatullin (1976) suggest that the parasitic relationships were established prior to the geographic separation of the North and South Atlantic forms of O. bartramii. 228 | ICES Cooperative Research Report No. 325 18.8.2 Environmental effects Zuev et al. (1976) reported that, in the Atlantic, these squid forage in the productive zones found seawards of upwelling areas, and concentrations can be found in the North Atlantic from the Canary Islands to Cape Blanc, around Madeira, and around the Azores. Lefkaditou et al. (2011) attributed the apparent increase in abundance of this species in recent years in the Mediterranean to warming of upper sea layers since the 1980s. 18.9 Fisheries Although this species is fished primarily in the Pacific (for details see Bower and Ichii, 2005), there are estimated to be 2.5 million t of O. bartramii in the North Atlantic (Nigmatullin, 1989; Nigmatullin et al., 1991). In the ICES Area, landings of O. bartramii are reported as mixed landings together with I. coindetii, Todaropsis eblanae, and Todarodes sagittatus. Although Spanish landings of this group have reached several thousand tonnes in some years, it is unlikely that much of this biomass is attributable to O. bartramii. Nigmatullin (1989, 2004) notes that consistently occurring concentrations of O. bartramii have not been found in the North Atlantic, and it is, therefore, unlikely to represent a viable fishery resource in this area. 18.10 Stock identity The North Pacific population of O. bartramii consists of two stocks that are spatially separated on the feeding grounds, reproduce at different times and which have recently exhibited opposite trends in abundance (Chen and Chiu, 2003; Chen, 2010). There is no evidence yet to suggest that the North Atlantic population consists of more than one stock, but there is a general lack of research on this species in the North Atlantic. 18.11 Future research, needs, and outlook Much of the basic biology of O. bartramii in the North Atlantic is not known. Considering that several authors (see above) consider the North Atlantic population to be a separate subspecies, it is not appropriate to assume that data from the Pacific populations are representative of the North Atlantic. The translation of the comprehensive Russian literature from the 1960s to 1990s on oceanic ommastrephid squids into English would supply a wealth of new information to the international scientific community. Cephalopod biology and fisheries in Europe: II. Species Accounts Cephalopod biology and fisheries in European waters: species accounts Gonatus fabricii Boreoatlantic armhook squid | 229 230 | 19 ICES Cooperative Research Report No. 325 Gonatus fabricii (Lichtenstein, 1818) Uwe Piatkowski, Karsten Zumholz, Patrizia Jereb, Sonia Seixas, Daniel Oesterwind, Evgenia Lefkaditou, A. Louise Allcock, Graham J. Pierce, and Oleg Katugin Common names Encornet atlantoboreal (France), gonalura atlantoboreal (Spain), Boreoatlantic gonate squid or Boreoatlantic armhook squid (UK) (Figure 19.1). Synonyms Onychoteuthis fabricii Lichtenstein, 1818, Onychoteuthis amoena Möller, 1842, Cheloteuthis rapax Verrill, 1881 in 1880–1881. See Kristensen (1981a) for full details of synonomy. 19.1 Geographic distribution The boreoatlantic gonate squid, Gonatus fabricii (Lichtenstein, 1818), is widely distributed in offshore Arctic and subArctic waters of the North Atlantic, and its distribution also extends into the western Barents Sea (Arctic Ocean). In the Northeast Atlantic, it is found in the Norwegian Sea, westwards around Greenland to Baffin Bay and the Newfoundland Basin, and southwards to southern Cape Cod in Figure 19.1. Gonatus fabricii. Ventral the Northwest Atlantic (Nesis, 1971; Wiborg, view. From Kristensen (1981a). 1979b; Kristensen, 1981a, 1983; Bjørke and Gjøsæter, 2004; Roper et al., 2010b; Golikov et al., 2013) (Figure 19.2). Cephalopod biology and fisheries in Europe: II. Species Accounts | 231 Figure 19.2. Gonatus fabricii. Geographic distribution in the North Atlantic. 19.2 Taxonomy 19.2.1 Systematics Coleoidea – Decapodiformes – Oegopsida – Gonatidae – Gonatus. 19.2.2 Type locality Amerdloq Fjord, Holsteinsborg (ca. 67°N 54°W), West Greenland, 457–521 m [fide Kristensen and Knudsen (1983)]. 19.2.3 Type repository Kobenhavns Universitet, Zoologisk Museum, Universitetsparken 15, DK 2100 Copenhagen, Denmark. Neotype [fide Kristensen (1981a: 66)]. 19.3 Diagnosis 19.3.1 Paralarvae Paralarvae are characterized by the presence of a pair of round or oblong chromatophores on the ventral surface of the head, slightly anterior to the ocular axis, and by a dorsal pad on the funnel organ with an inverted V-shape, with straight lateral sides (Kristensen, 1981a; Falcon et al., 2000). The presence of chromatophores can be used as the primary character to identify even very small specimens (ML <3.6 mm), in which the funnel organ is too small to verify confidently its shape (Falcon et al., 2000). The onset of formation of hooks from suckers, both on the tentacular clubs and arms I–III, is at ML >20 mm (Falcon et al., 2000). This seems to be a good character to define the end of what is now termed the paralarval phase and the beginning of the juvenile phase in gonatids (Young, 1972; Kristensen, 1977a); in fact, the presence of hooks is likely to indicate a change in feeding habits and, therefore, a change in the ecological position of the squids. 232 | ICES Cooperative Research Report No. 325 19.3.2 Juveniles and adults Figure 19.3. Gonatus fabricii. Tentacular club showing the two larger hooks. Photo: Karsten Zumholz. In juveniles, one large hook is generally present on the club, with three small hooks proximal to it and a moderately large hook distal to it (see Figure 19.3); several small suckers are present on both dorsal and ventral sides of the club, especially at the proximal end, where they form a large cluster (Kristensen, 1977a; Falcon et al., 2000). Adult maximum mantle length is 385 mm, which was reported for a female in the Barents Sea (Sennikov et al., 1989), although the largest individual recorded by Arkhipkin and Bjorke (2000) was 322 mm ML. The mantle is long, slender, conical, slightly wider at its midpoint, tapering to a sharp point posteriorly, its muscular part ending at the conus, with a fleshy, tapered column extending posteriorly as the tail. Fins are heart-shaped, with anterior lobes free and lateral margins rounded, their length <50% of ML, their width slightly less than their length. Tentacular Figure 19.4. Gonatus fabricii. Lower beak clubs are small and slender, their length ca. (left) and upper beak (right). Photo: Uwe 12–20% of ML, with one very large, central Piatkowski. hook followed proximally by three small hooks and distally by one moderately large hook. Nine to 13 tetraserial rows of suckers and hooks are present on the proximal half of arms III, and 14–17 tetraserial rows of suckers (no hooks) on the proximal half of arms IV (Kristensen, 1981a; Roper et al., 2010b). Note that tetraserial armature on the arms is characteristic of the Gonatidae (Roper et al., 1969). Beaks are illustrated in Figure 19.4. 19.4 Remarks Gonatus fabricii and G. streenstrupi are similar species, and confusion between the two may arise in areas of the (North) Atlantic where they overlap, such as the Irminger Sea (Kristensen, 1981a). Whereas G. fabricii is thought to be the most abundant squid in the high latitudes of the Atlantic and the only native pelagic squid in the Arctic (Nesis, 2001; Golikov et al., 2013), G. steenstrupi lives in the boreal zone of the Atlantic, especially in the eastern part off the United Kingdom, Ireland, and Spain (Kristensen, 1981a). Gonatus steenstrupi was also the most abundant squid in a comprehensive collection of oceanic cephalopods from an RV “G. O. Sars” expedition in summer 2004 to the northern and central regions of the Mid-Atlantic Ridge, including the Reykjanes Ridge and the Charlie Gibbs Fracture Zone (Vecchione et al., 2010). The two species can be separated on the basis of the two large chromatophores present on the ventral surface of the head in G. fabricii, and absent in G. steenstrupi; this character can also be used to distinguish paralarvae of the two species (Falcon et al., 2000; Vecchione and Young, 2006). Other useful characters to separate the two species are the numbers of tentacular club hooks proximal to the large central hook: three hooks in G. fabricii, 4–5 hooks (the largest is the most distal) in G. steenstrupi (Kristensen, Cephalopod biology and fisheries in Europe: II. Species Accounts | 233 1981a). A possible complication is mentioned by Boyle (2009). Vecchione and others participating in the RV “G. O. Sars” expedition in 2004 (Vecchione et al., 2010) found several specimens in which one tentacular club displayed the characteristics of G. fabricii, whereas the other club was consistent with G. steenstrupi. Boyle suggests that genetic studies are needed to resolve the issue. Kristensen (1981a) also mentioned the relative size of the club as a potentially useful character: G. fabricii has a relatively smaller club [12–20% of pen length (PL)], and G. steenstrupi has a relatively larger club (20–35% of PL). As noted by Arkhipkin and Bjorke (1999), G. fabricii has a muscular “tail” at the posterior end of the mantle; hence, ML exceeds PL by ca. 13%. This tail is often damaged in trawl-caught animals, making it impossible to measure their dorsal mantle length. Hence, PL is often used as the standard measurement. 19.5 Life history The life cycle of G. fabricii probably does not exceed 2 years. Spawning takes place from winter to summer, and females die soon after egg development is completed. 19.5.1 Egg and juvenile development Eggs are translucent, light blue, and roughly spherical (elliptical), with maximum egg diameter of 4–6 mm (Kristensen, 1981b; Bjørke and Hansen, 1996; Bjørke et al., 1997). Nesis (1999) suggests that embryonic development takes ca. 4 months. However, this conclusion is based on a formula developed for warm-water species, and the real development time may be much longer (O. Katugin, pers. comm.). Hatching size is ca. 3 mm ML (see Figure 19.5). Paralarvae may be found widely in the water column, but usually at depths <400 m in spring and mainly within the upper 100 m in summer (Falcon et al., 2000). Juveniles are found in Figure 19.5. Gonatus fabricii. large shoals in the uppermost 100 m of the water colEgg and hatchling. Egg diameumn over deep water (Nesis, 1965). South of the polar ter 5.5 mm. Photo: Lars Are circle, juveniles are reported to perform upward diurHamre (from Bjørke and Gjøsæter, 2004). nal migrations at night (Kristensen, 1977b). By the time the hook on the tentacular club starts to develop (20 mm ML), the adult proportions of the body become recognizable. At that stage, the squids are very mobile and swim like adults (Kristensen, 1977b). 19.5.2 Growth and lifespan As in other squid species (e.g. Illex coindetii, Jereb and Ragonese, 1995; Arkhipkin et al., 1998), different methods to investigate growth and age give different results for G. fabricii. Analysis of length frequency data suggests a rather long life cycle (2–3 years, Muus, 1962; Zumholz and Frandsen, 2006). Slow growth rates of 4–5 mm (Piatkowski and Wieland, 1993; Zumholz and Frandsen, 2006) and 8–9 mm month–1 (Kristensen 1977b, 1984) were proposed for animals from West Greenland waters. This would not be so unlikely for a polar species, given that cold-water species grow more slowly and live longer than species from lower latitudes. Statolith microstructure analysis of juveniles and immature squids revealed four growth zones, and daily, weekly, and fortnightly increment bands in the statoliths have been proposed (Kristensen, 1980). 234 | ICES Cooperative Research Report No. 325 If the assumption of 1 increment d–1 is true for G. fabricii, as has been shown for other species, based on the total number of increments counted in adult specimens, the lifespan would not exceed 2 years (Arkhipkin and Bjørke, 2000). Sources differ as to whether the length–weight relationship differs between sexes. Arkhipkin and Bjorke (2000) reported no differences, whereas Zumholz and Frandsen (2006) found sexual dimorphism in the growth pattern (Table 19.1). Table 19.1. Gonatus fabricii. Length–weight relationships in different geographic areas for females (F), males (M), and sexes combined (All). Original equations converted to W = aMLb, where W is body mass (g) and ML is dorsal mantle length (cm). Region a B Sex Reference West Greenland 0.269 2.050 F Zumholz and Frandsen (2006) 0.053 2.648 M 0.101 2.412 All 0.138 2.43 All Kristensen (1984) 0.118 2.47 All Arkhipkin and Bjørke (1999) Norwegian Sea 19.5.3 Maturation and reproduction Many aspects of the biology of this species have been described only relatively recently. As noted by Bjørke (2001), only seven mature specimens had been recorded and only one described in detail. Development of the testis begins at a pen length of ca. 80–100 mm, and maturity is reached at a pen length of ca. 200 mm (Kristensen, 1983). Spermatophores measure 6– 10 mm. The ovary begins to develop at a pen length of 60–90 mm and increases in weight until maturity. Spermatophores have been found attached onto the buccal membrane of maturing and ripe females, indicating head-to-head copulation (Arkhipkin and Bjørke, 1999; Zumholz and Frandsen, 2006). Individual fecundity is estimated to be ca. 10 000. Female G. fabricii undergo considerable degenerative changes before spawning; the tentacles are lost, the arm and mantle tissues swell, the suckers on the arms are lost, and the animals lose their capability for active locomotion. It has been hypothesized (Arkhipkin and Bjørke, 1999) that these degenerative changes are related to the important activity of the nidamental glands in these species, i.e. the secretion of a peculiarly dense matter that envelops the eggs within the egg mass; this, in turn, would make the egg masses negatively buoyant, and bound to sink unless they are carried in the arms of “brooding”, light, and positively buoyant females. Gonatus onyx females are known to “brood” their eggs (Okutani et al., 1995; Seibel et al., 2000, 2005). Females use hooks on their arms to hold the egg mass, apparently contracting and extending the arms repeatedly to aerate the eggs (Siebel et al., 2005). This may also be the case in G. fabricii. Bjorke et al. (1997) caught egg masses and mature females together in pelagic trawls and speculates that females may have been egg brooding. Adult mature male G. fabricii show no signs of degeneration and seem likely to mate several times during their life cycle (Kristensen, 1984). It is speculated that the squid spawn in the Norwegian Sea from winter to summer and that the eggs hatch from late March to June or July (Bjørke and Gjøsæter, 2004). Spawning is suggested to take place at great depths, in oceanic waters. As noted above, females probably brood the eggs, although free egg masses have been found among Cephalopod biology and fisheries in Europe: II. Species Accounts | 235 spent females, possibly because the egg masses had become detached from the females during capture. The eggs are kept together in a single layer between two mucous membranes (Bjørke et al., 1997; Bjørke and Gjøsæter, 2004). Off Greenland in the Davis Strait, hatching is believed to take place in spring and early summer, whereas the eggs hatch in Disko Bay in autumn and early winter (Kristensen, 1984). 19.6 Biological distribution 19.6.1 Habitat Gonatus fabricii is an oceanic species that exists commonly between the surface and 500– 1000 m; records from depths of 2700 m exist, however. Adults are common at the bottom and in midwater layers in Arctic and subArctic waters, whereas juveniles live within a very wide range of depths from 2000 m to the surface, to where they may undertake diel migrations. Adults hunting for prey near the surface at night are reported from West Greenland (Kristensen, 1981b, 1983; O. Katugin, pers. comm.). 19.6.2 Migrations This species undertakes vertical migrations and, possibly, horizontal migrations. Kristensen (1977b) reports dispersal of young squid by the West Greenland Current from zone 1 to zone 2, although no other extensive horizontal migrations are reported. Variation in the barium:calcium ratio in the statoliths of this species suggests that juveniles inhabit surface waters and that larger specimens move to deeper waters. In addition, increases in the uranium:calcium and strontium:calcium ratios towards the outer part of the statolith suggested migration of adult squid into colder water (Zumholz et al., 2007b). 19.7 Trophic ecology 19.7.1 Prey Juveniles feed on copepods, euphausiids, amphipods, pteropods, and chaetognaths (Table 19.2). Adults can feed on prey larger than themselves (Kristensen, 1984), and the diet consists of macroplanktonic crustaceans (amphipods, euphausiids), fish [e.g. capelin (Mallotus villosus), redfish (Sebastes marinus), and lanternfish], and cephalopods (occasionally including bottom-dwellers such as octopuses). Cannibalism also takes place (Nesis, 1965; Zuev and Nesis, 1971; Wiborg, 1980; Kristensen, 1984). Although crustaceans are the main prey of both juveniles and adults, the importance of fish and cephalopods in the diet increases with age. Fish start to become more important in the diet after the hooks on the tentacular clubs have developed (Kristensen, 1984). Table 19.2. Prey composition of Gonatus fabricii, as known from studies in different regions of the eastern Atlantic (compiled from Nesis, 19651; Zuev and Nesis, 19712; Wiborg; 19803, 19824, 19845; Kristensen, 19846). Taxon Species Osteichthyes Myctophidae indet. lanternfish2 Sternoptychidae Maurolicus muelleri (pearlside)4 Osmeridae Mallotus villosus (capelin)6 Sebastidae Sebastes norvegicus (as S. marinus) (redfish or rose fish)3 Crustacea Decapoda Pasiphaea sp.6, indet. shrimps3,6 236 | ICES Cooperative Research Report No. 325 Euphausiacea Meganyctiphanes norvegica3,4,5, Thysanoessa longicaudata1, indet.2 Mysida indet.6 Amphipoda Hyperia galba1, Hyperiidae indet.6, Parathemisto abyssorum4, Parathemisto spp.3,4,5, Pseudalibrotus spp.1, Themisto gaudichaudi (as P. gaudichaudii)4, T. libellula (as P. libellula)4, indet.3 Isopoda indet.3,6 Copepoda Calanus finmarchicus1,3,4,5, C. hyperboreus1,3, Euchaeta sp.5, Paraeuchaeta norvegica1,3,4, Metridia spp.1, Temora sp.5, indet.3 Cephalopoda Gonatus fabricii2,3,4,6, Octopoda indet.2, Oegopsida indet.2, indet.6 Gastropoda Clione limacina3, Limacina retroversa (retrovert pteropod)1,3,4,5 Chaetognatha Eukrohnia spp.3,4,5, Sagitta spp.1,3,4,5 19.7.2 Predators Gonatus fabricii is one of the most abundant food resources for virtually all top predators in the North Atlantic (Bjørke, 2001; Bjørke and Gjøsæter, 2004; Table 19.3) and a key species in the eastern Arctic foodweb (Gardiner and Dick, 2010). It is taken by large pelagic cephalopods and fish, seabirds, and marine mammals (Table 19.3). Beaks in stomach contents of predators are often only identified to genus (i.e. Gonatus sp.), and the inference that it is G. fabricii that has been eaten then depends to some extent on knowledge of its distribution and abundance. However, as noted above under Remarks, the distribution overlaps with that of G. steenstrupii, and both species are found around Iceland and southeast Greenland (see maps in Frandsen and Zumholz, 2004; Jereb and Roper, 2010), so there is scope for misidentification. Table 19.3. Known predators of Gonatus fabricii in the North Atlantic. Taxon Species References Cephalop- European flying squid (Toda- Wiborg (1972) oda rodes sagittatus) Osteichthyes Atlantic cod (Gadus morhua) Grimpe (1933) Atlantic salmon (Salmo salar) Lear (1980) Deep water arrowtooth eel (His- Martin and Christiansen (1997) tiobranchus bathybius) Greater amberjack (Seriola Matallanas et al. (1995) dumerili) Greenland halibut (Reinhardtius Dawe et al. (1998), Hovde et al. (2002), hippoglossoides) Michalsen et al. (1998) Redfish (Sebastes marinus) Nesis (1965) Roundnose grenadier (Cory- Bergstad et al. (2010) phaenoides rupestres) Aves Atlantic puffin (Fratercula arc- Falk et al. (1992) tica) Pinnipedia Common murre (Uria aalge) Barrett et al. (1997) Northern fulmar (Fulmarus glaci- Lydersen et al. (1989), Garthe et al. alis) (2004) Thick-billed murre (Uria lomvia) Barrett et al. (1997) Harp seal (Phoca groenlandica) Lydersen et al. (1991), Potelov et al. (2000), Haug et al. (2004) Cephalopod biology and fisheries in Europe: II. Species Accounts Cetacea | 237 Hooded seal (Cysophora cris- Potelov et al. (2000), Bjørke (2001), tata) Haug et al. (2004) Blue whale (Balaenoptera mus- Hjort and Ruud (1929) culus) Northern bottlenose whale (Hy- Benjaminsen and Christensen (1979), peroodon ampullatus) Clarke and Kristensen (1980), Lick and Piatkowski (1998), Bjørke and Gjøsæter (1998), Bjørke (2001), Hooker et al. (2001), Santos et al. (2001c) Cuvier’s beaked whale (Ziphius Blanco et al. (1997), Santos et al. cavirostris) (2001d) Long-finned pilot whale (Globi- Nesis (1965), Desportes and Mouritsen cephala melas) (1988, 1993), Bjørke (2001) Narwhale (Monodon monoc- Grimpe (1933), Laidre and Heide- eros) Jørgensen (2005) Sperm whale (Physeter macro- Clarke and Macleod (1976), Clarke cephalus) (1997), Bjørke and Gjøsæter (1998), Santos et al. (1999, 2002), Bjørke (2001), Simon et al. (2003), Mendes et al. (2007) 19.8 Fisheries Gonatus fabricii is considered to have some fishery potential. It is the most abundant squid of the Arctic and subArctic waters of the North Atlantic, it has a high lipid content, the flesh, at least of younger animals, has a good consistency, and the species attains a desirable size (Nesis, 1965; Wiborg, 1979b; Kristensen, 1984; Frandsen and Wieland, 2004; Roper et al., 2010b). According to Kristensen (1984), the very high lipid content of the digestive gland (ca. 63%) makes it suitable for industrial use as well, although the abundance of lipases in the midgut may be problematic (see Okuzumi and Fujii, 2000). Piatkowski and Wieland (1993) suggested that the species might be of commercial interest, based on the abundance of early life stages of G. fabricii off West Greenland. Bjørke and Gjøsæter (1998) suggested that there was surplus production of this species in the Norwegian Sea, which could be exploited by the fisheries. However, because females undergo significant tissue degradation as they mature (Arkhipkin and Bjorke, 1999), fisheries might logically target immature animals, although it is possible that mature females could be marketed for animal feeds, while retaining males for human consumption. As noted by Frandsen and Wieland (2004), there have been at least two unsuccessful experimental fisheries for this species. In 1998, an experimental fishery targeted adult G. fabricii in the Norwegian Sea using a pelagic trawl, but catches were small (no more than 10 kg haul–1). An experimental bottom-trawl fishery for cephalopods conducted off West Greenland during a period of two months in 2003 achieved a total catch of oegopsid squid (probably Gonatus sp.) of only 4.7 kg. However, G. fabricii is used by Greenland Inuit as bait in the cod and shellfish fisheries and for human food. It is also regularly taken as bycatch in shrimp trawls in Greenland (Frandsen and Wieland, 2004; Roper et al., 2010b). 19.9 Stock identity Off West Greenland, at least two distinct populations exist (Disko Bay and Davis Strait), with differences in time of spawning and morphometric measurements (Kristensen, 1982). Another, probably separate, population is found in the Norwegian Sea 238 | ICES Cooperative Research Report No. 325 (Bjørke and Gjøsæter, 2004). However, genetic methods for stock separation have not yet been applied to G. fabricii. 19.10 Future research, needs, and outlook Considering the possible fishery potential of this species, improved knowledge on distribution, aggregation patterns, and migrations would be useful. Molecular genetic identification of remains in predator stomach contents would supplement the (incomplete) information on identity available from beaks. Cephalopod biology and fisheries in Europe: II. 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A., Fernández, R., Ieno, E., Porteiro, F., et al. 2004. Variability in the diet of common dolphins (Delphinus delphis) in Galician waters 1991– 2003 and relationship with prey abundance. ICES Document CM 2004/Q: 09. 40 pp. Shimko, B. 1992. Ageing and biological peculiarities of Todarodes sagittatus (Lamarck). ICES Document CM 1992/K: 12. 12 pp. Villanueva, R., and Sánchez, P. 1989. Some data on the biology of the squid Todarodes angolensis (Cephalopoda: Ommastrephidae) in Namibian waters. Selected Papers of the International Commission for the Southeast Atlantic Fisheries, 1: 17–22. Warneke-Cremer, C. 1986. Beiträge zur Systematik und Verbreitung der ommastrephiden Tintenfische (Mollusca, Cephalopoda, Teuthoidea) im Atlantik aufgrund der Fänge des FFS 'Walther Herwig' 1966 und 1968. Mitteilungen aus dem Institut für Seefischerei der Bundesforschungsanstalt für Fischerei, Hamburg, 40: 1–116. Wiborg, K. F. 1972. The squid Todarodes sagittatus (Lamarck). Norwegian investigations in the Norwegian Sea and North Atlantic waters 1970–1972. ICES Document CM 1972/K: 25. 13 pp. Wiborg, K. F. 1978. Squid, Todarodes sagittatus (Lamarck) in Norwegian coastal waters during the autumn 1977 and spring 1978. ICES Document CM 1978/K: 16. 12 pp. Wiborg, K. F. 1980. The squid Todarodes sagittatus (Lamarck). Immigration and occurrence at the Norwegian coast and adjacent ocean areas from the autumn 1979 to the spring 1980. Fisken og Havet 3: 13–27 [in Norwegian, with English abstract]. Wiborg, K. F. 1981. Akkar Todarodes sagittatus (Lamarck). Norwegian investigations, April–December 1980. Fisken og Havet 2: 31–45 [in Norwegian, with English abstract]. 334 | ICES Cooperative Research Report No. 325 Wiborg, K. F., and Beck, I. M. 1983. Squid Todarodes sagittatus (Lamarck) distribution and biology in northern waters, August 1982–June 1983. ICES Document CM 1983/K: 7. 15 pp. Wiborg, K. F., and Gjøsæter, J. 1981. The squid Todarodes sagittatus (Lamarck). Distribution and biology in northern waters, April 1980–April 1981. ICES Document CM 1981/K: 14. 18 pp. Wiborg, K. F., Gjøsæter, J., Beck, I. M., and Fossum, P. 1983. Squid Todarodes sagittatus (Lamarck) distribution and biology in northern waters, April 1982–June 1983. ICES Document CM 1983/K: 7. 15 pp. Zumholz, K., and Piatkowski, U. 2002. Beak length analysis of Loligo forbesi, Todarodes sagittatus and Todaropsis eblanae from the northern North Sea. Bulletin of Marine Science, 71: 1146. 20.2.16 Todaropsis eblanae Ayensa, M. G., Montero, M. P., Borderias, A. J., Hurtado, J. L. 2002. Influence of some protease inhibitors on gelation of squid muscle. Journal of Food Science, 67: 1636–1641. Burukovsky, R. N., Gaevskaya A. V., Domanevski L. N., Nigmatullin, Ch. M., and Panfilov, B. G. 1979. Main results of the research on squid carried out by the AtlantNIRO in the centraleast Atlantic. ICES Document CM 1979/K: 2. 24 pp. Dillane, E., Galvin, P., Coughlan, J., Rodhouse, P. 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Elemental distribution in cephalopod statoliths: NanoSIMS provides new insights into nano-scale structure. Reviews in Fish Biology and Fisheries, 17: 487–491. 340 | ICES Cooperative Research Report No. 325 Annex 1: European and Mediterranean common names for cephalopods Evgenia Lefkaditou, Roger Villanueva, Tooraj Valinassab, and Graham J. Pierce This annex lists common names for cephalopods used in Europe and in non-European countries bordering the Mediterranean. These countries and their associated languages and dialects covered are listed in Table A1.1, along with the abbreviations used. Unless otherwise indicated, only the main official language is listed for each country. Abbreviations follow the ISO 639-2 codes as listed on the Library of Congress Standards webpage (http://www.loc.gov/standards/iso639-2/php/code_list.php). Some languages have different codes for bibliographic and terminology purposes. The material has been compiled from various published general accounts (e.g. Jaeckel, 1958; Roper et al., 1984; Jereb and Roper, 2005, 2010) and national lists, as well as information from colleagues and web sources, as listed in Table A1.2. The common names of cephalopods appear in Table A1.3. Gaps indicate where we (and our listed sources) were unaware of common names for the species–country combinations in question. We can rarely be completely certain that no common name exists in these cases. We have not attempted to include all colloquial names (e.g. “inks” for squid in Scotland). We also excluded some names because their use is generic or ambiguous, such as the Icelandic “kolkrabbi” (octopus or flying squid) and “smockfiskur” (squid or cuttlefish) or the Norwegian “blekksprut” (octopus, cuttlefish, or sepiolid). However, we have included generic names where they were apparently the only name in use (e.g. kalamari for squid species in Israel). In the case of Arabic names, we list the most frequently used common names. Additional regularly used names in the Arabic-speaking countries are listed in Table A1.4. Table A1.1. Names and codes of countries and languages (including widely spoken dialects) used along Mediterranean and Northeast Atlantic coasts. Some countries have two codes, here identified as "B" (bibliographic) or "T" (terminology). Country Code Language or dialect Name ISO 639-2 Name Code English translation AL Albania Alb Gjuha shqipe Albanian BE Belgium Dut Belgisch-Nederlands 5 Belgian Dutch, Flemish CS Serbia-Mon- Srp Srpski Serbian tenegro CY Cyprus ell-cyp Ελληνικά Cypriot Greek CZ Czech Re- ces (T); cze Čeština Czech public (B) Germany deu (T); ger Deutsch German DE (B) DK Denmark Dan Dansk Danish DZ Algeria Ara ‫ال عرب ية‬ Arabic EG Egypt Ara ‫ال عرب ية‬ Arabic 5 The other official languages are French and German. Cephalopod biology and fisheries in Europe: II. Species Accounts ES Spain Cat Català | 341 Catalan; Valencian ES Spain Spa Español; Castellano Spanish; Castilian ES Spain eus (baq) Euskara Basque ES Spain Glg Galego Galician FI Finland Fin Suomi Finnish FO Faroe Islands Fao Føroyskt Faroese FR France fra (T); fre(B) Français French FR France Cos Corse Corsican FR France Bre Breton Breton FR France Mah Marsall Marshallese GB United King- Eng English English (UK) dom GR Greece ell (gre) Ελληνικά Greek HR Croatia Hrv Hrvatski Croatian IE Ireland Gle Gaeilge Irish IL Israel Heb Ivrit Hebrew IS Iceland ice (B); isl(T) Íslenska Icelandic IT Italy Ita Italiano Italian IT Italy Scn Sicilianu Sicilian IT Italy Srd Sardu Sardinian LB Lebanon Ara ‫ال عرب ية‬ Arabic LV Latvia Lav Latviešu valoda Latvian LY Libya Ara ‫ال عرب ية‬ Arabic MA Morocco Ara ‫ال عرب ية‬ Arabic MT Malta Mlt Malti Maltese NL Netherlands nld (T); dut (B) Nederlands Dutch; Flemish NO Norway Nor Nynorsk 6 Norwegian PL Poland Pol Polski Polish PT Portugal Por Português Portuguese RU Russia Rus Russkij jazyk Russian SE Sweden Swe Svenska Swedish SI Slovenia Slv Slovenščina (slovenski Slovenian jezik) SY Syria Ara ‫ال عرب ية‬ Arabic TN Tunisia Ara ‫ال عرب ية‬ Arabic TR Turkyie Tur Türkçe Turkish 6 Norway has three official written languages, Bokmål, Nynorsk, and Sami. 342 | ICES Cooperative Research Report No. 325 Table A1.2. Additional sources for the common names listed in Table A1.3: published works, web resources, and communications from colleagues. Country Albania Source Dhora (2008). Fjalor i emrave të kafshëve të Shqipërisë (Emri shkencor – Shqip – Anglisht) / Dictionary of animal names of Albania (Scientific names – Albanian – English). Camaj – Pipa. Shkodër, Albania. pp. 288. (Cited at WoRMS - World Register of Marine Species - http://www.marinespecies.org/index.php). Algeria Wahid Refes, Ecole Nationale Supιrieure des Sciences de la Mer et de l'Amιnagememt du Littoral (ENSSMAL), Campus universitaire de Dιly Ibrahim, Alger, Algerie. Belgium Dutch: WoRMS (see above), confirmed by Jan Mees, Director of Flanders Marine and The Institute, Belgium. Netherlands Croatia Svjetlana Krstulović Šifner, Head of the Center of Marine Studies, University of Split, and Slo- Croatia. venia Cyprus Cypriot Greek: Charis Charilaou, Department of Fisheries and Marine Research, Ministry of Agriculture, Nicosia, Cyprus. Denmark Ministry of Food, Agriculture and Fisheries, Danish Veterinary and Food Administration (March 2011) Egypt Official Egyptian language: Hatem Hanafy Mahmoud, National Institute of Oceanography and Fisheries (NIOF), Kasr El-Ainy Street, Cairo, Egypt. In Arabic from Bariche (2012). Faroe Is- Eilif Gaard, Faroe Marine Research Institute, Box 3051, FO-110 Torshavn, Faroe Is- lands lands. Finland Petri Suuronen, Finnish Game and Fisheries Research Institute, FI-00791 Helsinki, Finland. France Breton and Corsican language: Jean-Paul Robin, IBFA- Université de Caen BasseNormandie Esplanade de la paix, Caen Cedex, France; Mediterranean French (Marshallese) : Angélique Jadaud, IFREMER, Sète Cedex, France. Greece Hellenic Statistical Authority http://www.statistics.gr/portal/page/portal/ESYE, except * which are unofficial names mentioned in the Pan-European Species directory Infrastructure (PESI) portal (http://www.eu-nomen.eu/portal) and ** which are names proposed to the Hellenic Ministry of Rural Development and Food, General Directorate for Fisheries common names, to be adapted as official common names. Iceland Jorge Fernandez, University of Aberdeen, UK Ireland Irish Statute Book, Office of the Attorney General, Ireland (March 2011) http://www.irishstatutebook.ie/2003/en/si/0320.html Israel Italy Dor Edelist, Marine Ecologist, Haifa University, Israel. Official Italian language: Bello and Borri (1990), except for * Roper et al. (2010); common names in Sicilian dialect provided by Fabio Fiorentino, Istituto per l'Ambiente Marino Costiero (IAMC), Mazara del Vallo, Sicily; common names in Sardinian dialect from the southern part of the island provided by Rita Cannas, University of Cagliari, Department of Life Sciences and Environment, Cagliari, Sardinia, Italy. Latvia Georgs Kornilovs, Institute of Food Safety, Animal Health and Environment "BIOR", Department of Fish Resources Research, Riga, Latvia. Malta Constantine Mifsud, Maltese taxonomist of molluscs. Norway Moen and Svendsen (1999), Gjøsæter et al. (2009), Terje van der Meeren, Institute of Marine Research, Austevol, Norway. Cephalopod biology and fisheries in Europe: II. Species Accounts Portugal | 343 Ministério da Agricultura, do Desenvolvimento Rural e das Pescas, Portugal; Sanches(1989). Russia Chingis Nigmatullin, Atlantic Research Institute of Fisheries and Oceanography, Kaliningrad, Russia. Spain Basque, Catalan, Galician: Ministerio de Medio Ambiente y Medio Rural y Marino, Gobierno de España Sweden Francesca Vitale, Swedish University of Agricultural Sciences (SLU), Department of Aquatic Resources, Institute of Marine Research, Lysekil, Sweden. Syria and Arabic dialects: Bariche (2012). Tunisia Turkey Alp Salman, Ege University, Faculty of Fisheries, Department of Hydrobiology, Izmir, Turkey. 344 | ICES Cooperative Research Report No. 325 Table A1.3. Common names of cephalopod species in different languages and dialects most widely spoken along Mediterranean and Northeast Atlantic coasts. Where specific and more generic common names are listed, the latter are given in parenthes. Notes: (*) and (**) indicate names taken from different sources, as listed under the relevant country in Table A1.2. Language Ara AL-sqi Octopus vulgaris Eledone cirrhosa Eledone moschata Sepia officinalis Sepia elegans Sepia orbignyana ‫اخطبوط شانع‬ ‫اخطبوط اقرن‬ ‫اخطبوط مسكي‬ ‫سيبيا شائع‬ ‫سيبيا انيق‬ ‫سيبيا زهري‬ Octopod i eger Sepia; supja; sipa; Sepja elegante Tetëkëmbëshi; liku- sepja rishtja; oktapodi i zakonshëm; BE-dut Kraak; gewone Kleine achtarm Gewone zeekat; Sierlijke zeekat Gedoornde zeekat Kleine sepie, Dornsepie zeekat octopus; gewone achtarm; achtarm CS-srp Hobotnica CY-ell Oχταπόδι CZ-ces Chobotnice Muzgavac Crni muzgavac Mοσχοχτάποδο Σουπιά (soupia) Sépie obecná pobřežní DE-deu Gemeiner krake, Zirrenkrake Moschuskrake Gemeiner tintenfisch oktopus DK-dan schlammsepie Almindelig Eledoneblæksprutte; ele- ottearmet done Moskusblæksprutte Sepiablæksprutte; sepia blæksprutte; ottearmet blæksprutte ES-cat Pop roquer Pop blanc Pop mesquer Sèpia Castanyó ES-spa Pulpo Pulpo blanco Pulpo almizclado, pulpo Choco, jibia, sepia Choquito, castaño cabezón Choquito picudo Cephalopod biology and fisheries in Europe: II. Species Accounts ES-eus Olagarro, amor- | 345 Cabezón Txautxa, jibia rotza ES-glg Polbo Polbo cabezón Polbo almiscrado Choco FI-fin Meritursas Pikkumyskitursas Myskitursas Yleinen mustekala, se- Choquiño Choquiño picudo Seiche élégante Seiche rosée pia FO-fao FR-fra Pieuvre, poulpe Elédone commune, Elédone musquée Seiche commune poulpe, poulpe blanc FR-bre Soavenn, morgazh Morgad, margatte FR-cos Polpu, pulpu, Seppia porpu FR-mah Poufre Poulpe Poulpe Seiche Sépions Sépions GB-eng Common octopus Horned octopus, lesser Dusky octopus Common cuttlefish Elegant cuttlefish Pink cuttlefish Μοσκιός (moschios) Σουπιά (soupia) Crni muzgavac Sipa octopus Χταπόδι (chta- Μοσκιός (moschios); podi) λασπομοσχιός** HR-hrv Hobotnica Bijeli muzgavac IE-gle Ochtapas IL-heb Tamnoon hakhof GR-ell Κοκκινοσουπιά* Sipica rumenka Sipica iglata Sabiddah Sabiddah Seppia elegante Seppia pizzuta Castagnola Castagnola Cudal Tamnoon Tamnoon hamooshk Dyonon rokhim (sabiddah) IS-ice IT-ita Mokkur Polpo commune Moscardino bianco Moscardino muschiato, Seppia comune moscardino rosso IT-scn Purpu majulinu Purpu jancu Purpu nivuru Siccia Siccitedda Castagnola IT-srd Pruppu Pruppu biancu Pruppu muscau Seppia Seppia Seppia 346 | LV-lav ICES Cooperative Research Report No. 325 Parastais Mazais astoņkājis Baltais astoņkājis Parastā sēpija Elegantā sēpija Sārtā sēpija Frajjell tal-frilli Qarnita ta-misk Siċċa Siċċa tat-tkarkir Siċċa tax-xewka Sierlijke zeekat Gedoornde zeekat Choco-vulgar, choco Choco-elegante Choco-de-cauda Sepia orbinji astoņkājis MT-mlt Qarnita NL-nld Kraak; gewoone Inktwise; zeekat; octopus; gewone gewone zeekat; achtarm; achtarm gewone inktvis NO-nor Blekksprut Vanlig åttearmet bleksprut PL-pol Ośmiornica Matwa zwyczajna; zwyczajna PT-por matwa pospolita Polvo-vulgar, Polvo-do-alto; polvo- Polvo-mosqueado, polvo cabeçudo polvo-de-cheiro, polvo cabeçudo RU-rus Obyknovennayj Obyknovennayj malyj Muskusnyj os'minog; Obyknovennaya kara- Izjaschnaya kara- os'minog os'minog мускусный осьминог katiza or sepia katiza or sepia Åttaarmad bläck- Eledone, åttaarmad fisk bläckfisk SI-slv Hobotnica Kodrasta hobotnica Moškatna hobotnica Sipa Mala sipa Bodičasta sipa TR-tur Ahtapot Mis ahtapot; kancalı ahta- Misk ahtapotu Sübye, mürekkep balığı Küçük sübye, Dikenli sübye, mürekkep balığı mürekkep balığı SE-swe pot Sepia Cephalopod biology and fisheries in Europe: II. Species Accounts Language Sepietta ow- Sepiola atlantica Sepiola spp. | 347 Loligo vulgaris Loligo forbesii Alloteuthis media eniana Ara ‫حبار ابتر شائع‬ Alloteuthis subulata ‫حبار ابتر‬ ‫حبار ابتر‬ AL-sqi ‫حبار مالوف‬ ‫حبار اورده‬ ‫حبار خيزراني‬ ‫حبار اورده‬ Kallamari; lignja; kalmari; ulignja BE-dut Langwerpige Kleine zeekat, dwerginktvis gewone Dwerginktvis Gewone pijlinktvis; Noordse pijlinktvis Kleine pijlinktvis, pijlinktvis dwergpijlinktvis dwerginktvis, dwerginktvis CS-srp CY-ell καλαμάρι CZ-ces Krakatice DE-deu Große sepiette Atlantische sepi- Gemeiner kalmar Nordischer kalmar ole Großkeuliger mit- Geschwänzter At- telländischer zwer- lantischer zwer- gkalmar gkalmar, gepfriemter zwergkalmar DK-dan Europæisk loligo; Eu- Loligoblæksprutte; ropæisk loligoblæk- loligo Dværgblæksprutte sprutte ES-cat ES-spa Calamar Globitos Gobitos Globitos Calamar, calamar Calamarsó Calamar veteado Calamarín menor Calamarín picudo Lura colorada Puntilla pequena Puntilla común europeo ES-eus ES-glg Txipiron Chopiños Lura 348 | ICES Cooperative Research Report No. 325 FI-fin Pikkuseepia FO-fao Lítil høgguslokkur FR-fra Kalmari pikkukalmari, pohjanmerenkalmari Mathøgguslokkur Sépiole com- Sépiole grandes Encornet eu- mune oreilles ropéenne FR-bre Encornet veiné Casseron bambou Casseron comun Encornet Encornet Piste; chipiron Piste; chipiron European squid Veined squid Midsize squid European com- Stivell, stiogenn, sifoc'h FR-cos Totanu FR-mah GB-eng GR-ell HR-hrv Sépions Common bob- Atlantic bobtail tail squid squid mon squid Είδος Είδος σεπιέττας** Σεπίολας** Obični bobić Καλαμάρι Καλαμαράκι* Ψευτοκαλάμαρο* Lignja IE-gle Καλαμάρι; Lignja pučinka Lignjica Šiljasta lignja Mathair shuigh na heorpa IL-heb Sabiddah Sabiddah Loligo shakoof (kala- Kalamari mari) IS-ice IT-ita Evrópskur smokkfiskur Seppiola com- Seppiola Calamaro comune Calamaro venato mune IT-scn Confettura Confettura cappuccettu cappuccettu Calamaretto co- Calamaretto mune puntuto Calamaru Calamaru Calamaricchi Calamaricchi IT-srd Seppiedda Seppiedda Seppiedda Calamari Calamari Calamareddu Calamareddu LV-lav Strupā sepieta Atlantijas sepiola Sepiola Parastais kalmārs Garspuru kalmārs Vidējais kalmārs Eiropas kalmārs MT-mlt Dakkru Dakkru Klamar Klamar Totlu Totlu tal-fond Cephalopod biology and fisheries in Europe: II. Species Accounts NL-nld | 349 Langwerpige Kleine zeekat; Pijlinktvis; gewone dwerginktvis gewone pijlinktvis Noordse pijlinktvis Kleine pijlinktvis; dwergpijlinktvis dwerginktvis; dwerginktvis NO-nor PL-pol PT-por kałamarnice Chopo-anão Chopo-anão Chopo-anão Lula-comum, lula- Lula-riscada Lula-bicuda-curta Lula-bicuda-comprida vulgar, lula-legítima, lula RU-rus SE-swe Sepietta ow- Atlantichrskaya Obyknovennayj Severnyj dlinnoperyj Allotevtis or ena sepiola dlinnoperyj kal'mar kal'mar dlinnohvostyj kal'mar Sepietta Atlantsepiola kalmar Nordisk kalmar SI-slv TR-tur Kulaklı sübye Sipice Ligenj Kulaklı sübye Kalamar Alloteuthis Pritlikavi ligenj Kalamar Orta boy kalamar; Küçük kalamar 350 | Language ICES Cooperative Research Report No. 325 Ommastrephes bar- Illex coindetii Todarodes sagittatus Todaropsis eblanae Gonatus fabricii References ‫حبار احمر‬ ‫حبار طيار‬ ‫حبار طيار صغير‬ ‫ح بار‬ Bariche (2012) tramii Ara ‫حبار‬ AL-sqi BE-dut Dhora ( 2008) Purperen pijlinktvis Grote pijlinktvis Kromme pijlinktvis Adema et al. (1989) CS-srp CY-ell θράψαλο θράψαλο βυθού kurzflossenkalmar Europäischer flugkalmar CZ-ces DE-deu Kleiner flugkalmar Nordischer köderkalmar DK-dan Rød blæksprutte Flyveblæksprutte ES-cat Canana vera Canana Volador Volador Pota costera ES-eus Pota Pota Pota ES-glg Pota común ES-spa Pota saltadora FI-fin Pota pequena Euroopanliitokalmari European Commission (1998) FO-fao FR-fra Agnhøgguslokkur Encornet volant Encornet rouge Toutenon commun Toutenon soufleur Pisseur Pisseur Pisseur FR-bre FR-cos FR-mah Cephalopod biology and fisheries in Europe: II. Species Accounts GB-eng Neon flying squid Broadtail shortfin squid | 351 European flying squid Lesser flying squid Boreoatlantic gonate Roper et al. squid (1984), Jereb and Roper (2010) GR-ell θράψαλο; καταμάχι θράψαλο; κόκκινο θράψαλο πελαγικό; θράψαλο; ωκεανού ** θράψαλο καταμάχι* πλατύουρο θράψαλο ** HR-hrv Lignjavac Lignjun Lignjun veliki leteći lignjun IE-gle Office of the Attorney General, Ireland (2003) IL-heb Kalamari Kalamari Kalamari Kalamari Totano nero (*) Totano; todaro Totano viola Totano tozzo IS-ice IT-ita Bello and Borri (1990), Jereb and Roper (2010) IT-scn IT-srd Calamari Todaru di paranza Todaru di lenza Todaru di paranza Calamari calamari Calamari IS-ice LV-lav Marcialis (2005) Beitusmokkur Sarkanais kalmārs MT-mlt Totlu NL-nld Purperen pijlinktvis Īsspuru kalmārs Totlu Parastais lidotājkalmārs Mazais lidotājkal- Ziemeļatlantijas kal- mārs mārs Totlu Totlu Grote pijlinktvis Kromme pijlinktvis de Bruyne et al. (1994), Hayward et al. (1999), 352 | ICES Cooperative Research Report No. 325 Cattrijsse and Vincx (2001) NO-nor Akkar Gonatus Moen and Svendsen (1999), Gjøsæter et al. (2009) PL-pol PT-por RU-rus Pota-saltadora, Pota-voadora, potra- pota-de-orelhas voadora, charuto Kal'mar bartrama Evropejskij or severoatlan- Pota-europeia Pota-costeira Severnyj kal'mar strelka Sanches (1989) Korenastyj kal'mar Kal'mar - gonatus ticheskij korotkoperyj or kal'mar- severnyj kal'mar todaropsis As in RefsSEswe Kratkoplavuti ligenj Puščičasti ligenj Bartram (only in SE Erkek kalamar; Kirmizi kala- Erkek kalamar; mızraklı kala- Erkek kalamar; Turkey, fethiye) mar mar uçan kalamar SI-slv TR-tur Kalamar Bariche (2012) Cephalopod biology and fisheries in Europe: II. Species Accounts | 353 Table A1.4. Additional Arabic dialect names, adapted from Bariche (2012) except as indicated in Table A1.2 above. Species DZ EG Octopus vulgaris Karnite Okhtabute LB LY MA SY ‫رطالة‬ ‫أخطبوط‬ TN shaaea (‫) أخط بوط‬ Eledone cirrhosa Karnite hassi Eledone mos- Karnite hassi Okhtabute msky ‫خطبوطأ‬ ‫بومسك‬ ‫قرنيط مسكى‬ ‫رطال ةأ‬/‫خط بوط‬ ‫يأكسِم خط بوط‬ ‫بومسك‬ Shouibia Chubei; seiche; ‫ َحبَّار‬،‫صبيدج‬ Choubei; ‫ شوب اي‬/ (‫)خط بوط‬ chata Sepia; Sobbeit; ‫س ب يط‬ choubai /‫ س ب يا ح بار‬/ Sepia elegans Sepia ‫سبيط‬ Sepia orbig- Sepia Sepia officinalis ‫قرنيط ابيض‬ Sabbidije; ‫ ص ب يدج‬/‫ح بارا‬ ‫ سوب يا‬/ ‫ شواب ي‬/ ‫س ي ب يا‬ ‫ س ي ب يا‬/‫شوك و‬ ‫صبيضن بلدي‬/‫حبارا‬/‫صبيدج‬ ‫ َحبَّار‬،‫صبيدج‬ ‫شوابي صغير‬ ‫حبارا‬/‫صبيدج‬ ‫ َحبَّار‬،‫صبيدج‬ ‫شوابي صغير‬ ‫قلم صبيضن‬/‫قلم صبيدج‬/‫كاالمار‬ ‫فرنجي‬ ‫صبيدج‬ (‫)ك ل يماري‬ kalimary ‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫صبيدج‬ nyana Sepiolidae Sepia skhira Loligo vulgaris Calmar Loligo forbesii Calmar kalimary (‫)ك ل يماري‬ Alloteuthis media Calmar hassi ‫كليماري‬ ‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫َحبَّار َو َسطي‬ Alloteuthis subu- Calmar hassi ‫كليماري‬ ‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫َحبَّار أ وربي‬ Illex coindetii Calmar hmar Kalimary /‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫صبيضن كاوتشوك‬ ‫قلم‬ Todarodes sagit- Calmar hmar Kalimary; ‫ك ل يماري‬ ‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫كليماري‬ ‫َحبَّار طيار‬ Calmar hmar ‫كليماري‬ ‫قلم‬/‫قلم صبيدج‬/‫كاالمار‬ ‫كليماري‬ ‫َحبَّار طيار‬ lata tatus Todaropsis eblanae 354 | ICES Cooperative Research Report No. 325 Annex 2: Regression equations used to estimate cephalopod sizes based on measurements of beaks M. Begoña Santos and Graham J. Pierce In studies of diets of marine predator (e.g. predatory fish, seabirds, marine mammals), cephalopods are often identified from their chitinous mandibles, because cephalopod flesh digests relatively rapidly, and the beaks are indigestible and may persist in the stomach for several days (possibly due to becoming lodged in the stomach lining (see Clarke, 1986; Santos et al., 2001b). As beaks are often well preserved, with little evidence of size reduction attributable to digestion (Tollitt et al., 1997), measurements on the beaks can be used to estimate the original size of the cephalopods consumed. Squids and cuttlefish are generally identified from the lower beaks; consequently, most published regressions refer to lower beaks. Clarke (1986) gives regression equations for many species, but several other authors have subsequently compiled relevant regressions; these are all listed in Table A2.1. Additional regressions for Eledone cirrhosa are available in Lefkaditou and Bekas (2004), but they have not been included here because beak size is treated as the response variable and animal size as the predictor. For squids and cuttlefish, the usual measurement is rostral length, whereas hood length is used for octopods. The measurements taken are illustrated in Figure A2.1. Finally, we included regressions based on measurement of the cuttlebone in Sepia officinalis (from Almonacid Rioseco et al., 2009). Figure A2.1. Stereoscopic images of decapod lower beaks from Clarke (1986), indicating features of a typical beak. Measurements illustrated are (1) rostral length, (2) hood length, and (3) crest length. Cephalopod biology and fisheries in Europe: II. Species Accounts | 355 Table A2.1. Regression equations to estimate cephalopod sizes [ML, dorsal mantle length (mm); W, total weight (g)] from beak measurements: LHL, lower hood length; LRL, lower rostral length (mm); UHL, upper hood length; URL, upper rostral length; CL, cuttlebone length. Sources are as follows: AG, González (1994); Alm, Almonacid Rioseco et al. (2009); Br, Brown and Pierce (1998); Cl, Clarke (1986); Her, Hernández García (1995); PG, Pérez-Gándaras (1983); San, Santos (1998); Wf, Wolff (1984), Xav, Xavier et al. (2010). Where a regression refers to one sex only, this is indicated. Where known, sample size (n) and goodness of fit (r2) are given. The symbol * indicates combined data from more than one species. Species Mantle length (mm) n r2 Source Octopus vulgaris Eledone cirrhosa ML = 3.380 + LHL  26.570 211 - PG Eledona moschata ML = 22.242 + LHL  28.230 Sepia officinalis ML = –2.140 + LHL  21.890 53 - PG ML = 0.0005 + CL  2.7142(males) 320 0.98 Alm ML = 0.0004 + CL  2.7451(females) 106 0.98 Alm ML = 21.340 + LHL  13.560 166 - Sepietta oweniana ML = 22.060 + LHL  2.550 67 - Sepiola atlantica ML = 15.020 + LHL  0.750 Loligo vulgaris ML = –42.220 + LRL  84.274 Sepia elegans Body weight (g) n r2 Source W = 6.171858  LHL3.03000 108 - PG W = 5.365600  LHL2.85000 214 - PG* W = 8.250720  UHL2.33740 W = 7.980491  LHL3.146 Br Xav W = 0.123690  LHL4.06000 53 - PG PG W = 5.312168  LHL1.56000 166 - PG PG W = 4.711470  LHL0.74000 67 - PG PG* W = 1.491825  LHL0.35000 69 - PG* PG* W = 8.331137  LRL2.91000 33 - PG* Sepia orbignyana 60 129 - ML = 3.420 + URL  65.902 29 - San W = 12.335700  URL2.53290 29 - San ML = –42.220 + LRL  84.274 129 - PG* W = 19.10595  LRL2.39000 74 - PG* ML = –28.956 + URL  103.891 232 - San W = 31.09200  URL2.49712 233 - San Alloteuthis subulata ML = –30.990 + LRL  113.970 135 - PG* W = 7.389056  LRL2.75000 116 - PG Alloteuthis media ML = –30.990 + LRL  113.970 135 - PG* W = 3.234906  LRL2.47000 14 - Cl Loligo forbesi Illex coindetti 356 | Todaropsis eblanae Todarodes sagittatus Ommastrephes bar- ICES Cooperative Research Report No. 325 W = 3.089471  LRL2.73500 (males) 157 0.916 AG W = 2.664456  LRL2.88800 (females) 165 0.940 AG Her W = 3.460109  LRL2.60400 (males) 99 0.98 Her Her W = 3.714336  URL2.41900 (males) 99 0.98 Her LRL2.67500 (females) ML = 56.849  LRL0.705 (males) ML = 57.812  URL0.656 (males) ML = 52.557  LRL0.865 (females) 101 0.94 Her W = 3.339764  101 0.96 Her ML = 53.006  URL0.827 (females) 101 0.94 Her W = 3.420203  URL2.55800 (females) 101 0.96 Her W = 2.590886  URL2.70200 (males) 157 0.946 AG W = 2.420563  URL2.77500 (females) 165 0.950 AG PG W = 1.803988  LRL3.17000 194 - PG Her W = 2.227545  LRL2.80000 (males) 99 0.98 Her Her W = 1.732213  URL2.80200 (males) 55 0.91 Her Her W = 1.965998  LRL3.03300 (females) 59 0.96 Her URL2.91700 (female) ML = –10.320 + LRL  35.040 ML = 31.031  LRL0.953 (males) ML = 28.737  URL0.948 (males) ML = 25.953  LRL1.095 (females) ML = 24.963  URL1.055 (females) 99 99 194 55 55 59 0.92 0.92 0.92 0.88 0.97 59 0.95 Her W = 1.440096  59 0.95 Her ML = –11.300 + LRL  41.360 - - Cl W = 2.188027  LRL2.83000 - - Cl ML = 62.396  LRL0.740 (females) 94 0.91 Her W = 3.386849  LRL2.48500 (female) 94 0.90 Her ML = 62.465  URL0.728 (females) 94 0.91 Her W = 3.375016  URL2.44900 (female) 94 0.90 Her ML = 52.7 + LRL  276.1 - 0.96 Wf W = 735.095189  LRL2.0700 - 0.98 Wf 0.94 Wf W = 812.405825  URL2.15000 Cl* W = 0.520000  trami ML = 51.4 + URL  282.4 Gonatus fabricii ML = –43.400 + LRL  42.870 17 - LRL3.33000 Wf 20 - Cl* Cephalopod biology and fisheries in Europe: II. Species Accounts | 357 Author and editor contact information Editors Patrizia Jereb Author: Chapters 2–19 Istituto Superiore per la Protezione e la Ricerca Ambientale (ex ICRAM), Via Brancati 48/60, 00144 Roma, Italy patrizia.jereb@isprambiente.it pajereb@tin.it A. Louise Allcock Author: Chapters 2– 19 Martin Ryan Institute, National University of Ireland, Galway, University Road, Galway, Ireland louise.allcock@nuigalway.ie Evgenia Lefkaditou Author: Chapters 3–19, Annex 1 Institute of Marine Biological Resources and Inland Waters, Hellenic Centre for Marine Research, Ag. Kosmas, 16777 Helliniko, Athens, Greece teuthis@hcmr.gr Uwe Piatkowski Author: Chapters 3, 4, 9, 13, 16–19 GEOMAR, Helmholtz Centre for Ocean Research Kiel, Marine Ecology, Düsternbrooker Weg 20, 24105 Kiel, Germany upiatkowski@geomar.de Lee C. Hastie Author: Chapters 10, 12–14, 17, 18 Oceanlab, University of Aberdeen, Main Street, Newburgh, Aberdeenshire, AB41 6AA, UK l.c.hastie@abdn.ac.uk Graham J. Pierce Author: Chapters 2–5, 9–19, Annexes 1, 2 Oceanlab, University of Aberdeen, Main Street, Newburgh, Aberdeenshire, AB41 6AA, UK and CESAM & Departamento de Biologia, Universidade de Aveiro, 3810-193 Aveiro, Portugal g.j.pierce@abdn.ac.uk g.j.pierce@ua.pt Authors Cleopatra Alidromiti Chapter 14 Fisheries Research Institute, Hellenic Argicultural Organization “DEMETER”, Hellenic Ministry of Rural Development and Food, Nea Peramos, 64007, Kavala, Greece cleopatraalidromiti@hotmail.com Eduardo Balguerias Chapters 3, 5 Instituto Español de Oceanografía, C/ Corazón de María 8, 28002 Madrid, Spain eduardo.balguerias@md.ieo.es director@md.ieo.es Paola Belcari Chapters 4, 9, 15, 17 Dipartimento Scienze Uomo e Ambiente, Via Derna 1, 56125 Pisa, Italy belcari@discat.unipi.it p.belcari@ucl.ac.uk 358| ICES Cooperative Research Report No. 325 Teresa Borges Chapter 4 Centre of Marine Sciences (CCMAR), University of Algarve, Campus de Gambelas, 8005-139 Faro, Portugal tborges@ualg.pt Manuel García Tasende Chapter 13 Servizo de Innovación Tecnolóxica da Acuicultura, Subdirección de Acuicultura, Secretaría Xeral do Mar, Consellería do Medio Rural e do Mar, Xunta de Galicia, Edificios Administrativos - San Caetano, s/n , 15781 Santiago de Compostela, Spain manuel.garcia.tasende@xunta.es Angel F. González Chapters 3, 11 Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain afg@iim.csic.es Ángel Guerra Chapters 3, 6, 10 Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain angelguerra@iim.csic.es José Iglesias Chapter 3 Instituto Español de Oceanografía, Centro Oceanográfico de Vigo, Apdo. 1552, 36200 Vigo, Spain jose.iglesias@vi.ieo.es Oleg Katugin Chapter 19 Pacific Research Fisheries Centre (TINRO-Centre), 4 Shevchenko Alley, Vladivostok 690090, Russia okatugin@mail.ru Noussithé Koueta Chapter 6 UMR-IFREMER, Physiologie et Ecophysiologie des Mollusques Marins, I.B.F.A., Université de Caen BasseNormandie, Esplanade de la Paix, 14032 Caen, Cedex, France noussithe.koueta@unicaen.fr Drosos Koutsoubas Chapters 6, 15 Department of Marine Sciences, Faculty of Environment, University of the Aegean, University Hill, 81100, Mytilini, Island of Lesvos, Greece drosos@aegean.gr and National Marine Park of Zakynthos, El. Venizelou 1 str., 29100 Zakynthos, Greece info@nmp-zak.org Ana Moreno Chapters 3, 5, 11, 13 IPMA, I.P. - Instituto Português do Mar e da Atmosfera, I.P., Av. Brasília s/n, 1449-006 Lisboa, Portugal amoreno@ipma.pt Daniel Oesterwind Chapters 13, 16, 19 Thünen Institute of Baltic Sea Fisheries, Alter Hafen Süd 2, 18069 Rostock, Germany daniel.oesterwind@ti.bund.de João Pereira Chapters 3, 11 IPMA, I.P. - Instituto Português do Mar e da Atmosfera, I.P. , Av. Brasília s/n, 1449-006 Lisboa, Portugal jpereira@ipma.pt Cephalopod biology and fisheries in Europe: II. Species Accounts | 359 Jean-Paul Robin Chapters 6, 11 UMR BOREA Biologie des ORganismes et Ecosystèmes Aquatiques, MNHN, UPMC, UCBN, CNRS-7208, IRD-207, Université de Caen Basse-Normandie Esplanade de la Paix, CS 14032, 14032 Caen, Cedex 5, France jean-paul.robin@unicaen.fr Pilar Sánchez Chapter 3 Institut de Ciències del Mar, (CSIC), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain pilar@icm.csic.es M. Begoña Santos Annex 2 Instituto Español de Oceanografía, Centro Oceanográfico de Vigo, Apdo. 1552, 36200 Vigo, Spain m.b.santos@vi.ieo.es Paolo Sartor Chapters 4, 9, 17 Consorzio per il Centro Interuniversitario di Biologia Marina ed Ecologia Applicata "G. Bacci", Viale N. Sauro 4, I-57128 Livorno, Italy psartor@cibm.it Sonia Seixas Chapters 5, 7, 8, 11, 19 Universidade Aberta, Rua Escola Politécnica 147, 1269-001 Lisbon, Portugal and Institute of Marine Research, CIC, University of Coimbra, 3000 Coimbra, Portugal soniabseixas@gmail.com Jennifer M. Smith Chapter 12 University of Aberdeen, School of Biological Sciences, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland and Kasetsart University, Coastal Development Centre, 50 Phaholyothin Road, Chatuchak, Bangkok 10900, Thailand jennifer.smith@abdn.ac.uk Ignacio Sobrino Chapters 3, 5, 7, 8 Instituto Español de Oceanografía, Centro Oceanográfico de Cadiz, Muelle Pesquero de Cadiz, Apdo. 2609, 11006 Cadiz, Spain ignacio.sobrino@cd.ieo.es Antonio Sykes Chapter 6 CCMAR-CIMAR L.A., Centro de Ciencias do Mar do Algarve, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal asykes@ualg.pt Tooraj Valinassab Annex 1 Iranian Fisheries Research Organization, P.O. Box 14155-6116, Tehran, Iran t_valinassab@yahoo.com Roger Villanueva Chapters 3, 11, 15, Annex 1 Institut de Ciències del Mar, (CSIC), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain roger@icm.csic.es Sansanee Wangvoralak Chapter 12 360| ICES Cooperative Research Report No. 325 Department of Fishery Management, Faculty of Fisheries, Kasetsart University, 50 Ngam Wong Wan Road, Ladyaow, Chatuchak, Bangkok 10900, Thailand ffissnw@ku.ac.th Karsten Zumholz Chapters 16, 17, 19 karsten.zumholz@gmx.de